The transcription factor FOXL2 in ovarian function and dysfunction

Folia Histochemica et Cytobiologica

Volumn 47, Issue 5, 2009, Pages

  De Baere, Elfride ^a   Fellous, Marc ^b,c   Veitia, Reiner A ^c,d  

^a GHENT UNIVERSITY HOSPITAL   (Belgium)

^b INSTITUT COCHIN   (France)

^c UNIVERSITÉ PARIS DESCARTES   (France)

^d INSTITUT JACQUES MONOD   (France)

Author keywords

Blepharophimosis syndrome; FOXL2; Menopause; Oxidative stress; Premature ovarian failure

Indexed keywords

GONADORELIN RECEPTOR; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR FOXL2; UNCLASSIFIED DRUG; FORKHEAD TRANSCRIPTION FACTOR;

ALPHA CHAIN; ANIMAL MODEL; AUTOSOMAL DOMINANT DISORDER; BLEPHAROPHIMOSIS; BLEPHAROPHIMOSIS PTOSIS EPICANTHUS INVERSUS SYNDROME; EPICANTHUS; EYELID; GENE EXPRESSION; GENE MUTATION; GENETIC DISORDER; GENOTYPE PHENOTYPE CORRELATION; HUMAN; LOSS OF FUNCTION MUTATION; MOUSE; NONHUMAN; OVARY; OVARY FUNCTION; OVARY INSUFFICIENCY; PATHOGENESIS; PHENOTYPE; PREMATURE OVARIAN FAILURE; PTOSIS; REGULATORY MECHANISM; REVIEW; ANIMAL; MUTATION;

ANIMALS; FORKHEAD TRANSCRIPTION FACTORS; HUMANS; MUTATION; PHENOTYPE; PRIMARY OVARIAN INSUFFICIENCY;

EID: 75949092042     PISSN: 02398508     EISSN: None     Source Type: Journal    
DOI: 10.2478/v10042-009-0062-7     Document Type: Review

References (54)

1. Zlotogora J, Sagi M, Cohen T. The blepharophimosis, ptosis, and epicanthus inversus syndrome: delineation of two types. Am J Hum Genet. 1983; 35(5):1020-1027.
2. Crisponi L, Deiana M, Loi A, Chiappe F, Uda M, Amati P, Bisceglia L, Zelante L, Nagaraja R, Porcu S and others. The putative forkhead transcription factor FOXL2 is mutated in blepharophimosis/ptosis/epicanthus inversus syndrome. Nat Genet. 2001; 27(2):159-166.
3. Pailhoux E, Vigier B, Vaiman D, Servel N, Chaffaux S, Cribiu EP, Cotinot C. Ontogenesis of female-to-male sex-reversal in XX polled goats. Dev Dyn. 2002;224(1):39-50.
4. Cocquet J, Pailhoux E, Jaubert F, Servel N, Xia X, Pannetier M, De Baere E, Messiaen L, Cotinot C, Fellous M and others. Evolution and expression of FOXL2. J Med Genet. 2002; 39(12):916-921.
5. Pannetier M, Servel N, Cocquet J, Besnard N, Cotinot C, Pailhoux E. Expression studies of the PIS-regulated genes suggest different mechanisms of sex determination within mammals. Cytogenet Genome Res. 2003;101(3-4):199-205.
6. 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(11):1691-1704.
7. Kioussi C, Carriere C, Rosenfeld MG. A model for the development of the hypothalamic-pituitary axis: transcribing the hypophysis. Mech Dev. 1999;81(1-2):23-35.
8. 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(11):2796-2805.
9. Moumné 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(1-2):2-11.
10. D'haene B, Attanasio C, Beysen D, Dostie J, Lemire E, Bouchard Ph, 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. A distant deletion of a 7.4 kb fragment that harbours cis-regulators and that interacts with the FOXL2 promoter causes BPES. PLoS Genetics. 5(6):e1000522. Epub 2009 Jun 19.
11. 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(4):933-942.
12. 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(11):1171-1181.
13. 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(14):2053-2062.
14. 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(23):2795-2804.
15. Beysen D, De Paepe A, De Baere E. FOXL2 mutations and genomic rearrangements in BPES. Hum Mutat. 2009;30(2):158-169.
16. De Baere E, Dixon MJ, Small KW, Jabs EW, Leroy BP, Devriendt K, Gillerot Y, Mortier G, Meire F, Van Maldergem L and others. Spectrum of FOXL2 gene mutations in blepharophimosis- ptosis-epicanthus inversus (BPES) families demonstrates a genotype--phenotype correlation. Hum Mol Genet. 2001;10(15):1591-1600.
17. De Baere E, Beysen D, Oley C, Lorenz B, Cocquet J, De Sutter P, Devriendt K, Dixon M, Fellous M, Fryns JP and others. FOXL2 and BPES: mutational hotspots, phenotypic variability, and revision of the genotype-phenotype correlation. Am J Hum Genet. 2003;72(2):478-487.
18. Beysen D, Raes J, Leroy BP, Lucassen A, Yates JR, Clayton- Smith J, Ilyina H, Brooks SS, Christin-Maitre S, Fellous M and others. 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(2):205-218.
19. Beysen D, De Jaegere S, Mowat D, Laframboise R, Gillessen- Kaesbach G, Fellous M, Veitia RA, Boucard P, Touraine P, Leroy BP and others. Mutation in Brief: Identification of 34 novel and 56 known FOXL2 mutations in patients with Blepharophimosis syndrome. Human Mutation. 2008;29(11):E205-19.
20. Raile K, Stobbe H, Trobs RB, Kiess W, Pfaffle R. A new heterozygous mutation of the FOXL2 gene is associated with a large ovarian cyst and ovarian dysfunction in an adolescent girl with blepharophimosis/ptosis/epicanthus inversus syndrome. Eur J Endocrinol. 2005;153(3):353-358.
21. Nallathambi J, Moumne L, De Baere E, Beysen D, Usha K, Sundaresan P, Veitia RA. A novel polyalanine expansion in FOXL2: the first evidence for a recessive form of the blepharophimosis syndrome (BPES) associated with ovarian dysfunction. Hum Genet. 2007;121(1):107-112.
22. Ramirez-Castro JL, Pineda-Trujillo N, Valencia AV, Muneton CM, Botero O, Trujillo O, Vasquez G, Mora BE, Durango N, Bedoya G and others. Mutations in FOXL2 underlying BPES (types 1 and 2) in Colombian families. Am J Med Genet. 2002;113(1):47-51.
23. Moumne L, Fellous M, Veitia RA. Deletions in the polyAlanine- containing transcription factor FOXL2 lead to intranuclear aggregation. Hum Mol Genet. 2005; 14(23):3557-3564.
24. Dollfus H, Stoetzel C, Riehm S, Lahlou Boukoffa W, Bediard Boulaneb F, Quillet R, Abu-Eid M, Speeg-Schatz C, Francfort JJ, Flament J and others. Sporadic and familial blepharophimosis -ptosis-epicanthus inversus syndrome: FOXL2 mutation screen and MRI study of the superior levator eyelid muscle. Clin Genet. 2003; 63(2):117-120.
25. Udar N, Yellore V, Chalukya M, Yelchits S, Silva-Garcia R, Small K. Comparative analysis of the FOXL2 gene and characterization of mutations in BPES patients. Hum Mutat. 2003;22(3):222-228.
26. Nallathambi J, Laissue P, Batista F, Benayoun BA, Lesaffre C, Moumné L, Pandaranayaka PE, Usha K, Krishnaswamy S, Sundaresan P, Veitia RA. Differential functional effects of novel mutations of the transcription factor FOXL2 in BPES patients. Hum Mutat. 2008;29(8):E123-E131.
27. Caburet S, Demarez A, Moumne L, Fellous M, De Baere E, Veitia RA. Arecurrent polyalanine expansion in the transcription factor FOXL2 induces extensive nuclear and cytoplasmic protein aggregation. J Med Genet. 2004;41(12):932-936.
28. Benayoun BA, Caburet S, Dipietromaria A, Bailly-Bechet M, Batista F, Fellous M, Vaiman D, Veitia RA. The identification and characterization of a FOXL2 response element provides insights into the pathogenesis of mutant alleles. Hum Mol Genet. 2008;17(20):3118-3127.
29. Moumné 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(7):1010-1019.
30. Beysen D, Moumné L, Veitia RA, Peters H, Leroy BP, De Paepe A, De Baere E. Missense mutations in the forkhead domain of FOXL2 lead to subcellular mislocalisation, protein aggregation and impaired transactivation. Human Molecular Genetics. 2008b;17(13):2030-2038.
31. de Ru MH, Gille JJ, Nieuwint AW, Bijlsma JB, van der Blij JF, van Hagen JM. Interstitial deletion in 3q in a patient with blepharophimosis-ptosis- epicanthus inversus syndrome (BPES) and microcephaly, mild mental retardation an growth delay: clinical report and review of the literature. Am J Med Genet. 2005;15(137(1)):81-87.
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-ptosis-epicanthus inversus. Mutat Res. 2004;554(1-2):19-22.
33. Vincent AL, Watkins WJ, Sloan BH, Shelling AN. Blepharophimosis and bilateral Duane syndrome associated with a FOXL2 mutation. Clin Genet. 2005; 68(6):520-523.
34. Varghese B, Donnai D, Shalet SM. Isolated growth hormone deficiency and BPES. Endocrine abstracts. 2002;3:P13.
35. Wales JKH. Hypergonadotropic hypogonadism in a 3-yearold girl with blepharophimosis, ptosis, and epicanthus inversus syndrome. Hormone Research. 1998;50(6):341-341
36. Prueitt and Zinn. A fork in the road to fertility. Nat Genet. 2001;27(2):132-134.
37. 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(8):e43.
38. 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(8):555-557.
39. 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(8):729-733.
40. 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(12):2767-2770.
41. Laissue P, Besma Lakhal B, Benayoun B, Dipietromaria A, Braham R, Elghezal H, Philibert P, Saâd A, Sultan C, Fellous M, and Veitia RAV. Functional evidence implicating FOXL2 in non syndromic premature ovarian failure and in the regulation of the transcription factor OSR2. J Med Gen. In press.
42. Benayoun BA, Auer J, Caburet S, Veitia RA. The post-translational modification profile of the forkhead transcription factor FOXL2 suggests the existence of parallel processive/concerted modification pathways. Proteomics. 2008;8(15):3118-3123.
43. Benayoun BA, Batista F, Auer J, Dipietromaria A, L'Hôte D, De Baere E, Veitia RA. Positive and negative feedback regulates the transcription factor FOXL2 in response to cell stress: evidence for a regulatory imbalance induced by disease-causing mutations. Hum Mol Genet. 2009;18(4):632-644.
44. 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(1-2):93-111.
45. Govoroun MS, Pannetier M, Pailhoux E, Cocquet J, Brillard JP, Couty I, Batellier F, Cotinot C. Isolation of chicken homolog of the FOXL2 gene and comparison of its expression patterns with those of aromatase during ovarian development. Dev Dyn. 2004; 231(4):859-870.
46. Baron D, Cocquet J, Xia X, Fellous M, Guiguen Y, Veitia RA. An evolutionary and functional analysis of FoxL2 in rainbow trout gonad differentiation. J Mol Endocrinol. 2004; 33(3):705-715.
47. Nakamoto M, Matsuda M, Wang DS, Nagahama Y, Shibata N. Molecular cloning and analysis of gonadal expression of Foxl2 in the medaka, Oryzias latipes. Biochem Biophys Res Comm. 2006;344(1):353-361.
48. 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(7):3424-3433.
49. Batista F, Vaiman D, Dausset J, Fellous M, Veitia R. Potential targets of FOXL2, a transcription factor involved in craniofacial and follicular development, identified by transcriptomics. Proc Natl Acad Sci. 2007;104(9):3330-3335.
50. Espey LL, Norris C, Forman J, Siler-Khodr T. Effect of indomethacin, cycloheximide, and aminoglutethimide on ovarian steroid and prostanoid levels during ovulation in the gonadotropin-primed immature rat. Prostaglandins. 1989;38(5):531-539.
51. Lee K, Pisarska MD, Ko JJ, Kang Y, Yoon S, Ryou SM, Cha KY, Bae J. Transcriptional factor FOXL2 interacts with DP103 and induces apoptosis. Biochem Biophys Res Commun. 2005;336(3):876-881.
52. Brunet A, Bonni A, Zigmond MJ, Lin MZ, Juo P, Hu LS, Anderson MJ, Arden KC, Blenis J, Greenberg ME. Akt promotes cell survival by phosphorylating and inhibiting a Forkhead transcription factor. Cell. 1999;96(6):857-868.
53. Burgering BM, Medema RH. Decisions on life and death: FOXO Forkhead transcription factors are in command when PKB/Akt is off duty. J Leukoc Biol. 2003;73(6):689-701.
54. Agarwal A, Gupta S, Sharma R. Oxidative stress and its implications in female infertility - a clinician's perspective. Reprod Biomed Online. 2005;11(5):641-650.