Towards a functional classification of pathogenic FOXL2 mutations using transactivation reporter systems

Human Molecular Genetics

Volumn 18, Issue 17, 2009, Pages 3324-3333

  Dipietromaria, Aurélie ^a,b,c   Benayoun, Bérénice A ^a,b   Todeschini, Anne Laure ^a,b   Rivals, Isabelle ^d   Bazin, Claude ^a,b   Veitia, Reiner A ^a,b  

^a INSTITUT JACQUES MONOD   (France)

^b UNIVERSITÉ PARIS DESCARTES   (France)

^c UNIVERSITÉ PARIS SACLAY   (France)

^d PSL RESEARCH UNIVERSITY   (France)

Author keywords

[No Author keywords available]

Indexed keywords

FORKHEAD TRANSCRIPTION FACTOR; MUTANT PROTEIN; TRANSCRIPTION FACTOR FOXL2; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; AUTOSOMAL DOMINANT DISORDER; BLEPHAROPHIMOSIS PTOSIS EPICANTUS INVERSUS SYNDROME; CELLULAR DISTRIBUTION; CLASSIFICATION; CONTROLLED STUDY; CYTOPLASM; GENETIC ASSOCIATION; GENETIC RISK; GENETIC VARIABILITY; GENOTYPE PHENOTYPE CORRELATION; MISSENSE MUTATION; NONHUMAN; PREMATURE OVARIAN FAILURE; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN AGGREGATION; PROTEIN DOMAIN; REPORTER GENE; TRANSACTIVATION;

ANIMALS; CERCOPITHECUS AETHIOPS; COS CELLS; EYE ABNORMALITIES; FEMALE; FORKHEAD TRANSCRIPTION FACTORS; GENES, REPORTER; GENETIC TECHNIQUES; HUMANS; LUCIFERASES; MUTATION, MISSENSE; OVARIAN FAILURE, PREMATURE; PROTEIN TRANSPORT; TRANSCRIPTIONAL ACTIVATION;

EID: 68749103447     PISSN: 09646906     EISSN: 14602083     Source Type: Journal    
DOI: 10.1093/hmg/ddp273     Document Type: Article

References (39)

1. 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. Nat. Genet., 27, 159-166.
2. Carlsson, P. and Mahlapuu, M. (2002) Forkhead transcription factors: Key players in development and metabolism. Dev. Biol., 250, 1-23.
3. Cocquet, J., Pailhoux, E., Jaubert, F., Servel, N., Xia, X., Pannetier, M., De Baere, E., Messiaen, L., Cotinot, C., Fellous, M. et al. (2002) Evolution and expression of FOXL2. J. Med. Genet., 39 916-921.
4. Cocquet, J., De Baere, E., Gareil, M., Pannetier, M., Xia, X., Fellous, M. and Veitia, R.A. (2003) Structure, evolution and expression of the FOXL2 transcription unit. Cytogenet. Genome Res., 101, 206-211.
5. Crisponi, L., Uda, M., Deiana, M., Loi, A., Nagaraja, R., Chiappe, F., Schlessinger, D., Cao, A. and Pilia, G. (2004) FOXL2 inactivation by a translocation 171 kb away: Analysis of 500 kb of chromosome 3 for candidate long-range regulatory sequences. Genomics, 83, 757-764.
6. Ottolenghi, C., Omari, S., Garcia-Ortiz, J.E., Uda, M., Crisponi, L., Forabosco, A., Pilia, G. and Schlessinger, D. (2005) Foxl2 is required for commitment to ovary differentiation. Hum. Mol. Genet., 14 2053-2062.
7. Schmidt, D., Ovitt, C.E., Anlag, K., Fehsenfeld, S., Gredsted, L., Treier, A.C. and Treier, M. (2004) The murine winged-helix transcription factor Foxl2 is required for granulosa cell differentiation and ovary maintenance. Development, 131, 933-942.
8. Batista, F., Vaiman, D., Dausset, J., Fellous, M. and Veitia, R.A. (2007) Potential targets of FOXL2, a transcription factor involved in craniofacial and follicular development, identified by transcriptomics. Proc. Natl Acad. Sci. USA, 104, 3330-3335.
9. Pannetier, M., Fabre, S., Batista, F., Kocer, A., Renault, L., Jolivet, G., Mandon-Pepin, B., Cotinot, C., Veitia, R. and Pailhoux, E. (2006) FOXL2 activates P450 aromatase gene transcription: Towards a better characterization of the early steps of mammalian ovarian development. J. Mol. Endocrinol., 36, 399-413.
10. De Baere, E., Beysen, D., Oley, C., Lorenz, B., Cocquet, J., De Sutter, P., Devriendt, K., Dixon, M., Fellous, M., Fryns, J.P. et al. (2003) FOXL2 and BPES: Mutational hotspots, phenotypic variability, and revision of the genotype-phenotype correlation. Am. J. Hum. Genet. 72, 478-487.
11. Zlotogora, J., Sagi, M. and Cohen, T. (1983) The blepharophimosis, ptosis, and epicanthus inversus syndrome: Delineation of two types. Am. J. Hum. Genet., 35, 1020-1027.
12. Beysen, D., Moumne, L., Veitia, R., Peters, H., Leroy, B.P., De Paepe, A. and De Baere, E. (2008) Missense mutations in the forkhead domain of FOXL2 lead to subcellular mislocalisation, protein aggregation and impaired transactivation. Hum. Mol. Genet., 17, 2030-2038.
13. Beysen, D., Raes, J., Leroy, B.P., Lucassen, A., Yates, J.R., Clayton-Smith, J., Ilyina, H., Brooks, S.S., Christin-Maitre, S., Fellous, M. et al. (2005) 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., 77, 205-218.
14. De Baere, E., Dixon, M.J., Small, K.W., Jabs, E.W., Leroy, B.P., Devriendt, K., Gillerot, Y., Mortier, G., Meire, F., Van Maldergem, L. et al. (2001) Spectrum of FOXL2 gene mutations in blepharophimosis-ptosis-epicanthus inversus (BPES) families demonstrates a genotype-phenotype correlation. Hum. Mol. Genet., 10, 1591-1600.
15. Nallathambi, N., Laissue, P., Batista, F., Benayoun, B.A., Lesaffre, C., Moumné, L., Pandaranayaka, E., Usha, K., Krishnaswamy, S., Sundaresan, P. et al. (2008) Differential functional effects of novel mutations of the transcription factor FOXL2 in BPES patients. Hum. Mutat., 121, 107-112.
16. Coulam, C.B., Adamson, S.C. and Annegers, J.F. (1986) Incidence of premature ovarian failure. Obstet. Gynecol., 67, 604-606.
17. Goswami, D. and Conway, G.S. (2005) Premature ovarian failure. Hum. Reprod. Update, 11, 391-410.
18. Fraser, I.S., Shearman, R.P., Smith, A. and Russell, P. (1988) An association among blepharophimosis, resistant ovary syndrome, and true premature menopause. Fertil. Steril., 50, 747-751.
19. Panidis, D., Rousso, D., Vavilis, D., Skiadopoulos, S. and Kalogeropoulos, A. (1994) Familial blepharophimosis with ovarian dysfunction. Hum. Reprod., 9, 2034-2037.
20. Gallagher, J.C., Rapuri, P. and Smith, L. (2007) Falls are associated with decreased renal function and insufficient calcitriol production by the kidney. J. Steroid Biochem. Mol Biol, 103, 610-613.
21. Maturana, M.A., Irigoyen, M.C. and Spritzer, P.M. (2007) Menopause, estrogens, and endothelial dysfunction: Current concepts. Clinics, 62, 77-86.
22. Anderson, G.L., Judd, H.L., Kaunitz, A.M., Barad, D.H., Beresford, S.A., Pettinger, M., Liu, J., McNeeley, S.G. and Lopez, A.M. (2003) Effects of estrogen plus progestin on gynecologic cancers and associated diagnostic procedures: The Women's Health Initiative randomized trial. JAMA, 290, 1739-1748.
23. Beral, V. (2003) Breast cancer and hormone-replacement therapy in the Million Women Study. Lancet, 362, 419-427.
24. Christin-Maitre, S. (2008) The role of hormone replacement therapy in the management of premature ovarian failure. Nat. Clin. Pract. Endocrinol. Metab., 4, 60-61.
25. Benayoun, B.A., Caburet, S., Dipietromaria, A., Bailly-Bechet, M., Fellous, M., Vaiman, D. and Veitia, R.A. (2008) The identification and characterization of a FOXL2 response element provides insights into the pathogenesis of mutant alleles. Hum. Mol. Genet., 17, 3118-3127.
26. Benayoun, B.A., Batista, F., Auer, J., Dipietromaria, A., L'Hote, D., De Baere, E. and 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. Hum. Mol. Genet., 18, 632-644.
27. Caburet, S., Demarez, A., Moumne, L., Fellous, M., De Baere, E. and Veitia, R.A. (2004) A recurrent polyalanine expansion in the transcription factor FOXL2 induces extensive nuclear and cytoplasmic protein aggregation. J. Med. Genet., 41, 932-936.
28. Nishi, Y., Yanase, T., Mu, Y., Oba, K., Ichino, I., Saito, M., Nomura, M., Mukasa, C., Okabe, T., Goto, K. et al. (2001) Establishment and characterization of a steroidogenic human granulosa-like tumor cell line, KGN, that expresses functional follicle-stimulating hormone receptor. Endocrinology, 142, 437-445.
29. Beysen, D., De Jaegere, S., Amor, D., Bouchard, P., Christin-Maitre, S., Fellous, M., Touraine, P., Grix, A.W., Hennekam, R., Meire, F. et al. (2008) Identification of 34 novel and 56 known FOXL2 mutations in patients with Blepharophimosis syndrome. Hum. Mutat., 29, E205-E219.
30. Moumne, L., Batista, F., Benayoun, B.A., Nallathambi, J., Fellous, M., Sundaresan, P. and Veitia, R.A. (2008) The mutations and potential targets of the forkhead transcription factor FOXL2. Mol. Cell. Endocrinol., 282, 2-11.
31. Moumne, L., Fellous, M. and Veitia, R.A. (2005) Deletions in the polyAlanine-containing transcription factor FOXL2 lead to intranuclear aggregation. Hum. Mol. Genet., 14, 3557-3564.
32. Moumne, L., Dipietromaria, A., Batista, F., Kocer, A., Fellous, M., Pailhoux, E. and 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. Hum. Mol. Genet., 17, 1010-1019.
33. Berry, F.B., Tamimi, Y., Carle, M.V., Lehmann, O.J. and Walter, M.A. (2005) The establishment of a predictive mutational model of the forkhead domain through the analyses of FOXC2 missense mutations identified in patients with hereditary lymphedema with distichiasis. Hum. Mol. Genet., 14, 2619-2627.
34. Hovatta, O. (2005) Methods for cryopreservation of human ovarian tissue. Reprod. Biomed. Online, 10, 729-734.
35. von Wolff, M., Donnez, J., Hovatta, O., Keros, V., Maltaris, T., Montag, M., Salle, B., Sonmezer, M. and Andersen, C.Y. (2009) Cryopreservation and autotransplantation of human ovarian tissue prior to cytotoxic therapy - A technique in its infancy but already successful in fertility preservation. Eur. J. Cancer, 45, 1547-1553.
36. Wallin, A., Ghahremani, M., Dahm-Kahler, P. and Brannstrom, M. (2009) Viability and function of the cryopreserved whole ovary: In vitro studies in the sheep. Hum Reprod, doi:10.1093/humrep/dep060.
37. Anderson, R.A., Wallace, W.H. and Baird, D.T. (2008) Ovarian cryopreservation for fertility preservation: Indications and outcomes. Reproduction, 136, 681-689.
38. Higuchi, R., Krummel, B. and Saiki, R.K. (1988) A general method of in vitro preparation and specific mutagenesis of DNA fragments: Study of protein and DNA interactions. Nucleic Acids Res., 16, 7351-7367.
39. Hastie, T., Tibshirani, R. and Friedman, J. (2001) The Elements of Statistical Learning-data Mining, Inference and Prediction. Springer-Verlag.