The forkhead factor FOXL2: A novel tumor suppressor?

Biochimica et Biophysica Acta - Reviews on Cancer

Volumn 1805, Issue 1, 2010, Pages 1-5

  Benayoun, Bérénice A ^a,b   Kalfa, Nicolas ^c   Sultan, Charles ^c,d   Veitia, Reiner A ^a,b  

^a CNRS   (France)

^b UNIVERSITÉ PARIS DESCARTES   (France)

^c LAPEYRONIE HOSPITAL   (France)

^d HÔPITAL ARNAUD DE VILLENEUVE   (France)

Author keywords

Cancer; FOXL2; Granulosa cell; Ovary; Tumor suppressor

Indexed keywords

BCL2 RELATED PROTEIN A1; CYCLIN DEPENDENT KINASE INHIBITOR 2A; DEAD BOX PROTEIN; FORKHEAD TRANSCRIPTION FACTOR; PROTEIN LATS1; PROTEIN SERINE THREONINE KINASE; SIRTUIN; SMAD3 PROTEIN; TRANSCRIPTION FACTOR FOXL2; UNCLASSIFIED DRUG;

ARTICLE; CANCER GROWTH; CARCINOGENESIS; CELL CYCLE ARREST; DNA DAMAGE; GENE EXPRESSION; GENE FUNCTION; GENE INTERACTION; GENE MUTATION; GENETIC REGULATION; GRANULOSA CELL TUMOR; MALIGNANT TRANSFORMATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; SUPPRESSOR GENE;

EID: 75349095236     PISSN: 0304419X     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bbcan.2009.09.002     Document Type: Note

References (71)

1. Crisponi L., Deiana M., Loi A., Chiappe F., Uda M., Amati P., Bisceglia L., Zelante L., Nagaraja R., Porcu S., Ristaldi M.S., Marzella R., Rocchi M., Nicolino M., Lienhardt-Roussie A., Nivelon A., Verloes A., Schlessinger D., Gasparini P., Bonneau D., Cao A., and Pilia G. The putative forkhead transcription factor FOXL2 is mutated in blepharophimosis/ptosis/epicanthus inversus syndrome. Nat. Genet. 27 (2001) 159-166
2. Zlotogora J., Sagi M., and Cohen T. The blepharophimosis, ptosis, and epicanthus inversus syndrome: delineation of two types. Am. J. Hum. Genet. 35 (1983) 1020-1027
3. Gersak K., Harris S.E., Smale W.J., and Shelling A.N. A novel 30 bp deletion in the FOXL2 gene in a phenotypically normal woman with primary amenorrhoea: case report. Hum. Reprod. 19 (2004) 2767-2770
4. Harris S.E., Chand A.L., Winship I.M., Gersak K., Aittomaki K., and Shelling A.N. Identification of novel mutations in FOXL2 associated with premature ovarian failure. Mol. Hum. Reprod. 8 (2002) 729-733
5. Laissue P., Lakhal B., Benayoun B.A., Dipietromaria A., Braham R., Elghezal H., Philibert P., Saad A., Sultan C., Fellous M., and Veitia R. Functional evidence implicating FOXL2 in non syndromic premature ovarian failure and in the regulation of the transcription factor OSR2. J. Med. Genet. 46 (2009) 455-457
6. Cocquet J., De Baere E., Gareil M., Pannetier M., Xia X., Fellous M., and Veitia R.A. Structure, evolution and expression of the FOXL2 transcription unit. Cytogenet. Genome Res. 101 (2003) 206-211
7. Cocquet J., Pailhoux E., Jaubert F., Servel N., Xia X., Pannetier M., De Baere E., Messiaen L., Cotinot C., Fellous M., and Veitia R.A. Evolution and expression of FOXL2. J. Med. Genet. 39 (2002) 916-921
8. Beysen D., De Jaegere S., Amor D., Bouchard P., Christin-Maitre S., Fellous M., Touraine P., Grix A.W., Hennekam R., Meire F., Oyen N., Wilson L.C., Barel D., Clayton-Smith J., de Ravel T., Decock C., Delbeke P., Ensenauer R., Ebinger F., Gillessen-Kaesbach G., Hendriks Y., Kimonis V., Laframboise R., Laissue P., Leppig K., Leroy B.P., Miller D.T., Mowat D., Neumann L., Plomp A., Van Regemorter N., Wieczorek D., Veitia R.A., De Paepe A., and De Baere E. Identification of 34 novel and 56 known FOXL2 mutations in patients with blepharophimosis syndrome. Hum. Mutat. 29 (2008) E205-E219
9. Caburet S., Demarez A., Moumne L., Fellous M., De Baere E., and Veitia R.A. A recurrent polyalanine expansion in the transcription factor FOXL2 induces extensive nuclear and cytoplasmic protein aggregation. J. Med. Genet. 41 (2004) 932-936
10. Beysen D., Moumne L., Veitia R., Peters H., Leroy B.P., De Paepe A., and De Baere E. Missense mutations in the forkhead domain of FOXL2 lead to subcellular mislocalisation, protein aggregation and impaired transactivation. Hum. Mol. Genet. 17 (2008) 2030-2038
11. Moumne L., Dipietromaria A., Batista F., Kocer A., Fellous M., Pailhoux E., and Veitia R.A. 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 (2008) 1010-1019
12. Nallathambi J., Laissue P., Batista F., Benayoun B.A., Lesaffre C., Moumne L., Pandaranayaka P.E., Usha K., Krishnaswamy S., Sundaresan P., and Veitia R.A. Differential functional effects of novel mutations of the transcription factor FOXL2 in BPES patients. Hum. Mutat. 16 (2008) e123-e131
13. Dipietromaria A., Benayoun B.A., Todeschini A.L., Rivals I., Bazin C., and Veitia R.A. Towards a functional classification of pathogenic FOXL2 mutations using transactivation reporter systems. Hum. Mol. Genet. 18 (2009) 3324-3333
14. Moumne L., Batista F., Benayoun B.A., Nallathambi J., Fellous M., Sundaresan P., and Veitia R.A. The mutations and potential targets of the forkhead transcription factor FOXL2. Mol. Cell. Endocrinol. 282 (2008) 2-11
15. Schmidt D., Ovitt C.E., Anlag K., Fehsenfeld S., Gredsted L., Treier A.C., and Treier M. The murine winged-helix transcription factor Foxl2 is required for granulosa cell differentiation and ovary maintenance. Development 131 (2004) 933-942
16. Uda M., Ottolenghi C., Crisponi L., Garcia J.E., Deiana M., Kimber W., Forabosco A., Cao A., Schlessinger D., and Pilia G. Foxl2 disruption causes mouse ovarian failure by pervasive blockage of follicle development. Hum. Mol. Genet. 13 (2004) 1171-1181
17. Ottolenghi C., Omari S., Garcia-Ortiz J.E., Uda M., Crisponi L., Forabosco A., Pilia G., and Schlessinger D. Foxl2 is required for commitment to ovary differentiation. Hum. Mol. Genet. 14 (2005) 2053-2062
18. Fuller P.J., Verity K., Shen Y., Mamers P., Jobling T., and Burger H.G. No evidence of a role for mutations or polymorphisms of the follicle-stimulating hormone receptor in ovarian granulosa cell tumors. J. Clin. Endocrinol. Metab. 83 (1998) 274-279
19. Graves P.E., Surwit E.A., Davis J.R., and Stouffer R.L. Adenylate cyclase in human ovarian cancers: sensitivity to gonadotropins and nonhormonal activators. Am. J. Obstet. Gynecol. 153 (1985) 877-882
20. Amsterdam A., and Selvaraj N. Control of differentiation, transformation, and apoptosis in granulosa cells by oncogenes, oncoviruses, and tumor suppressor genes. Endocr. Rev. 18 (1997) 435-461
21. Fuller P.J., and Chu S. Signalling pathways in the molecular pathogenesis of ovarian granulosa cell tumours. Trends Endocrinol. Metab. 15 (2004) 122-128
22. Ligtenberg M.J., Siers M., Themmen A.P., Hanselaar T.G., Willemsen W., and Brunner H.G. Analysis of mutations in genes of the follicle-stimulating hormone receptor signaling pathway in ovarian granulosa cell tumors. J. Clin. Endocrinol. Metab. 84 (1999) 2233-2234
23. Mayr D., Hirschmann A., Marlow S., Horvath C., and Diebold J. Analysis of selected oncogenes (AKT1, FOS, BCL2L2, TGFbeta) on chromosome 14 in granulosa cell tumors (GCTs): a comprehensive study on 30 GCTs combining comparative genomic hybridization (CGH) and fluorescence-in situ-hybridization (FISH). Pathol. Res. Pract. 204 (2008) 823-830
24. Kappes S., Milde-Langosch K., Kressin P., Passlack B., Dockhorn-Dworniczak B., Rohlke P., and Loning T. p53 mutations in ovarian tumors, detected by temperature-gradient gel electrophoresis, direct sequencing and immunohistochemistry. Int. J. Cancer 64 (1995) 52-59
25. Liu F.S., Ho E.S., Lai C.R., Chen J.T., Shih R.T., Yang C.H., and Tsao C.M. Overexpression of p53 is not a feature of ovarian granulosa cell tumors. Gynecol. Oncol. 61 (1996) 50-53
26. King L.A., Okagaki T., Gallup D.G., Twiggs L.B., Messing M.J., and Carson L.F. Mitotic count, nuclear atypia, and immunohistochemical determination of Ki-67, c-myc, p21-ras, c-erbB2, and p53 expression in granulosa cell tumors of the ovary: mitotic count and Ki-67 are indicators of poor prognosis. Gynecol. Oncol. 61 (1996) 227-232
27. Fletcher J.A., Gibas Z., Donovan K., Perez-Atayde A., Genest D., Morton C.C., and Lage J.M. Ovarian granulosa-stromal cell tumors are characterized by trisomy 12. Am. J. Pathol. 138 (1991) 515-520
28. Kalfa N., Patte C., Orbach D., Lecointre C., Pienkowski C., Philippe F., Thibault E., Plantaz D., Brauner R., Rubie H., Guedj A.M., Ecochard A., Paris F., Jeandel C., Baldet P., and Sultan C. A nationwide study of granulosa cell tumors in pre- and postpubertal girls: missed diagnosis of endocrine manifestations worsens prognosis. J. Pediatr. Endocrinol. Metab. 18 (2005) 25-31
29. Kalfa N., Philibert P., Patte C., Ecochard A., Duvillard P., Baldet P., Jaubert F., Fellous M., and Sultan C. Extinction of FOXL2 expression in aggressive ovarian granulosa cell tumors in children. Fertil. Steril. 87 (2007) 896-901
30. Shah S.P., Kobel M., Senz J., Morin R.D., Clarke B.A., Wiegand K.C., Leung G., Zayed A., Mehl E., Kalloger S.E., Sun M., Giuliany R., Yorida E., Jones S., Varhol R., Swenerton K.D., Miller D., Clement P.B., Crane C., Madore J., Provencher D., Leung P., Defazio A., Khattra J., Turashvili G., Zhao Y., Zeng T., Glover J.N., Vanderhyden B., Zhao C., Parkinson C.A., Jimenez-Linan M., Bowtell D.D., Mes-Masson A.M., Brenton J.D., Aparicio S.A., Boyd N., Hirst M., Gilks C.B., Marra M., and Huntsman D.G. Mutation of FOXL2 in granulosa-cell tumors of the ovary. N. Engl. J. Med. 360 (2009) 2719-2729
31. Myatt S.S., and Lam E.W. The emerging roles of forkhead box (Fox) proteins in cancer. Nat. Rev. Cancer 7 (2007) 847-859
32. Ellsworth B.S., Burns A.T., Escudero K.W., Duval D.L., Nelson S.E., and Clay C.M. 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. 206 (2003) 93-111
33. Blount A.L., Schmidt K., Justice N.J., Vale W.W., Fischer W.H., and Bilezikjian L.M. FoxL2 and Smad3 coordinately regulate follistatin gene transcription. J. Biol. Chem. 284 (2009) 7631-7645
34. Kim S.G., Kim H.A., Jong H.S., Park J.H., Kim N.K., Hong S.H., Kim T.Y., and Bang Y.J. The endogenous ratio of Smad2 and Smad3 influences the cytostatic function of Smad3. Mol. Biol. Cell. 16 (2005) 4672-4683
35. Vijayachandra K., Higgins W., Lee J., and Glick A. Induction of p16ink4a and p19ARF by TGFbeta1 contributes to growth arrest and senescence response in mouse keratinocytes. Mol. Carcinog. 48 (2009) 181-186
36. Burdette J.E., Jeruss J.S., Kurley S.J., Lee E.J., and Woodruff T.K. Activin A mediates growth inhibition and cell cycle arrest through Smads in human breast cancer cells. Cancer Res. 65 (2005) 7968-7975
37. Lee K., Pisarska M.D., Ko J.J., Kang Y., Yoon S., Ryou S.M., Cha K.Y., and Bae J. Transcriptional factor FOXL2 interacts with DP103 and induces apoptosis. Biochem. Biophys. Res. Commun. 336 (2005) 876-881
38. Brunet A., Bonni A., Zigmond M.J., Lin M.Z., Juo P., Hu L.S., Anderson M.J., Arden K.C., Blenis J., and Greenberg M.E. Akt promotes cell survival by phosphorylating and inhibiting a forkhead transcription factor. Cell 96 (1999) 857-868
39. Burgering B.M., and Medema R.H. Decisions on life and death: FOXO forkhead transcription factors are in command when PKB/Akt is off duty. J. Leukoc. Biol. 73 (2003) 689-701
40. Zender L., Xue W., Zuber J., Semighini C.P., Krasnitz A., Ma B., Zender P., Kubicka S., Luk J.M., Schirmacher P., McCombie W.R., Wigler M., Hicks J., Hannon G.J., Powers S., and Lowe S.W. An oncogenomics-based in vivo RNAi screen identifies tumor suppressors in liver cancer. Cell 135 (2008) 852-864
41. Kumetz L., Khan S., Zarrini P., Trivax B., Kao L., and Pisarska M.D. FOXL2, a gene associated with premature ovarian failure, interacts with large tumor suppressor gene 1 (LATS1). ASRM 62nd Annual Meeting vol. 86, Sup1 (2006), Elsevier, New Orleans, LA, USA S11-S12 Fertil. Steril.
42. Pisarska M.D., Kuo F., Tang S., and Khan S. Forkhead L2 (FOXL2), a gene associated with premature ovarian failure, is likely regulated through phosphorylation. ASRM 63rd Annual Meeting vol. 88, Sup1 (2007), Elsevier, Washington, DC, USA S168 Fertil. Steril.
43. Xu T., Wang W., Zhang S., Stewart R.A., and Yu W. Identifying tumor suppressors in genetic mosaics: the Drosophila lats gene encodes a putative protein kinase. Development 121 (1995) 1053-1063
44. Kemp C.J. You don't need a backbone to carry a tumour suppressor gene. Nat. Genet. 21 (1999) 147-148
45. St John M.A., Tao W., Fei X., Fukumoto R., Carcangiu M.L., Brownstein D.G., Parlow A.F., McGrath J., and Xu T. Mice deficient of Lats1 develop soft-tissue sarcomas, ovarian tumours and pituitary dysfunction. Nat. Genet. 21 (1999) 182-186
46. Hansen L.L., Jensen L.L., Dimitrakakis C., Michalas S., Gilbert F., Barber H.R., Overgaard J., and Arzimanoglou I.I. Allelic imbalance in selected chromosomal regions in ovarian cancer. Cancer Genet. Cytogenet. 139 (2002) 1-8
47. Xia H., Qi H., Li Y., Pei J., Barton J., Blackstad M., Xu T., and Tao W. LATS1 tumor suppressor regulates G2/M transition and apoptosis. Oncogene 21 (2002) 1233-1241
48. Benayoun B.A., Auer J., Caburet S., and Veitia R.A. The post-translational modification profile of the forkhead transcription factor FOXL2 suggests the existence of parallel processive/concerted modification pathways. Proteomics 8 (2008) 3118-3123
49. Andreu-Vieyra C., Chen R., and Matzuk M.M. Conditional deletion of the retinoblastoma (Rb) gene in ovarian granulosa cells leads to premature ovarian failure. Mol. Endocrinol. 22 (2008) 2141-2161
50. Scambia G., Lovergine S., and Masciullo V. RB family members as predictive and prognostic factors in human cancer. Oncogene 25 (2006) 5302-5308
51. Pisarska M.D., Bae J., Klein C., and Hsueh A.J. Forkhead l2 is expressed in the ovary and represses the promoter activity of the steroidogenic acute regulatory gene. Endocrinology 145 (2004) 3424-3433
52. Pannetier M., Fabre S., Batista F., Kocer A., Renault L., Jolivet G., Mandon-Pepin B., Cotinot C., Veitia R., and Pailhoux E. FOXL2 activates P450 aromatase gene transcription: towards a better characterization of the early steps of mammalian ovarian development. J. Mol. Endocrinol. 36 (2006) 399-413
53. Ellsworth B.S., Egashira N., Haller J.L., Butts D.L., Cocquet J., Clay C.M., Osamura R.Y., and Camper S.A. FOXL2 in the pituitary: molecular, genetic, and developmental analysis. Mol. Endocrinol. 20 (2006) 2796-2805
54. Lamba P., Fortin J., Tran S., Wang Y., and Bernard D.J. A novel role for the forkhead transcription factor FOXL2 in activin A-regulated follicle-stimulating hormone beta subunit transcription. Mol. Endocrinol. 23 (2009) 1001-1013
55. Benayoun B.A., Batista F., Auer J., Dipietromaria A., L'Hote D., De Baere E., and Veitia R.A. 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 (2009) 632-644
56. Deng C.X. SIRT1, is it a tumor promoter or tumor suppressor?. Int. J. Biol. Sci. 5 (2009) 147-152
57. van Heemst D., den Reijer P.M., and Westendorp R.G. Ageing or cancer: a review on the role of caretakers and gatekeepers. Eur. J. Cancer. 43 (2007) 2144-2152
58. Batista F., Vaiman D., Dausset J., Fellous M., and Veitia R.A. Potential targets of FOXL2, a transcription factor involved in craniofacial and follicular development, identified by transcriptomics. Proc. Natl. Acad. Sci. U. S. A. 104 (2007) 3330-3335
59. Crosio C., Casciati A., Iaccarino C., Rotilio G., and Carri M.T. Bcl2a1 serves as a switch in death of motor neurons in amyotrophic lateral sclerosis. Cell Death Differ. 13 (2006) 2150-2153
60. Zhang C., Gao C., Kawauchi J., Hashimoto Y., Tsuchida N., and Kitajima S. Transcriptional activation of the human stress-inducible transcriptional repressor ATF3 gene promoter by p53. Biochem. Biophys. Res. Commun. 297 (2002) 1302-1310
61. Liuwantara D., Elliot M., Smith M.W., Yam A.O., Walters S.N., Marino E., McShea A., and Grey S.T. Nuclear factor-kappaB regulates beta-cell death: a critical role for A20 in beta-cell protection. Diabetes 55 (2006) 2491-2501
62. Ayala-Torres S., Zhou F., and Thompson E.B. Apoptosis induced by oxysterol in CEM cells is associated with negative regulation of c-myc. Exp. Cell. Res. 246 (1999) 193-202
63. Yoon S., Ha H.J., Kim Y.H., Won M., Park M., Ko J.J., Lee K., and Bae J. IEX-1-induced cell death requires BIM and is modulated by MCL-1. Biochem. Biophys. Res. Commun. 382 (2009) 400-404
64. Gonzalez S., Perez-Perez M.M., Hernando E., Serrano M., and Cordon-Cardo C. p73beta-Mediated apoptosis requires p57kip2 induction and IEX-1 inhibition. Cancer Res. 65 (2005) 2186-2192
65. Benayoun B.A., Dipietromaria A., Bazin C., and Veitia R.A. FOXL2: at the crossroads of female sex determination and ovarian function. In: Maiese K. (Ed). Forkhead transcription factors: vital elements in biology and medicine. (2009), Landes Biosciences, Austin, TX
66. Quereda V., Martinalbo J., Dubus P., Carnero A., and Malumbres M. Genetic cooperation between p21Cip1 and INK4 inhibitors in cellular senescence and tumor suppression. Oncogene 26 (2007) 7665-7674
67. Otsuka F., Moore R.K., Iemura S., Ueno N., and Shimasaki S. Follistatin inhibits the function of the oocyte-derived factor BMP-15. Biochem. Biophys. Res. Commun. 289 (2001) 961-966
68. Benayoun B.A., Caburet S., Dipietromaria A., Bailly-Bechet M., Fellous M., Vaiman D., and Veitia R.A. The identification and characterization of a FOXL2 response element provides insights into the pathogenesis of mutant alleles. Hum. Mol. Genet. 17 (2008) 3118-3127
69. Treier M., Gleiberman A.S., O'Connell S.M., Szeto D.P., McMahon J.A., McMahon A.P., and Rosenfeld M.G. Multistep signaling requirements for pituitary organogenesis in vivo. Genes Dev. 12 (1998) 1691-1704
70. Kioussi C., O'Connell S., St-Onge L., Treier M., Gleiberman A.S., Gruss P., and Rosenfeld M.G. Pax6 is essential for establishing ventral-dorsal cell boundaries in pituitary gland development. Proc. Natl. Acad. Sci. U. S. A. 96 (1999) 14378-14382
71. Korbonits M., and Carlsen E. Recent clinical and pathophysiological advances in non-functioning pituitary adenomas. Horm. Res. 71 Suppl 2 (2009) 123-130