The Transcriptional Targets of Mutant FOXL2 in Granulosa Cell Tumours

PLoS ONE

Volumn 7, Issue 9, 2012, Pages

  Rosario, Roseanne ^a   Araki, Hiromitsu ^a   Print, Cristin G ^a   Shelling, Andrew N ^a  

^a UNIVERSITY OF AUCKLAND   (New Zealand)

Author keywords

[No Author keywords available]

Indexed keywords

AROMATASE; COMPLEMENTARY DNA; CYCLIN DEPENDENT KINASE 6; CYCLIN DEPENDENT KINASE INHIBITOR 1A; CYCLIN DEPENDENT KINASE INHIBITOR 2A; PROTEIN C JUN; SMAD3 PROTEIN; SMALL INTERFERING RNA; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR FOXL2; TRANSCRIPTION FACTOR SOX4; TRANSCRIPTION FACTOR SOX9; TRANSFORMING GROWTH FACTOR BETA; UNCLASSIFIED DRUG;

ARTICLE; CANCER CELL CULTURE; CARCINOGENESIS; CELL DEATH; CELL PROLIFERATION; CONTROLLED STUDY; EXPRESSION VECTOR; FEMALE; GENE EXPRESSION REGULATION; GENE OVEREXPRESSION; GENE SILENCING; GRANULOSA CELL TUMOR; HUMAN; HUMAN CELL; MICROARRAY ANALYSIS; PROTEIN EXPRESSION; PROTEIN TARGETING; QUANTITATIVE ANALYSIS; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; SOMATIC HYPERMUTATION; TRANSCRIPTION INITIATION; WESTERN BLOTTING;

AROMATASE; CELL LINE, TUMOR; FEMALE; FORKHEAD TRANSCRIPTION FACTORS; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, NEOPLASTIC; GENE KNOCKDOWN TECHNIQUES; GRANULOSA CELL TUMOR; HUMANS; MUTATION; NEOPLASM PROTEINS; OVARIAN NEOPLASMS; PHOSPHOPROTEINS; RNA, SMALL INTERFERING; SIGNAL TRANSDUCTION; TRANSCRIPTION, GENETIC; TRANSCRIPTOME; TRANSFORMING GROWTH FACTOR BETA;

EID: 84867019003     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0046270     Document Type: Article

References (52)

1. Colombo N, Parma G, Zanagnolo V, Insinga A, (2007) Management of ovarian stromal cell tumors. J Clin Oncol 25: 2944-2951.
2. Jamieson S, Fuller PJ, (2012) Molecular Pathogenesis of Granulosa Cell Tumors of the Ovary. Endocrine Reviews 33: 109-144.
3. East N, Alobaid A, Goffin F, Ouallouche K, Gauthier P, (2005) Granulosa cell tumour: a recurrence 40 years after initial diagnosis. J Obstet Gynaecol Can 27: 363-364.
4. Pectasides D, Pectasides E, Psyrri A, (2008) Granulosa cell tumor of the ovary. Cancer Treat Rev 34: 1-12.
5. Fuller PJ, Chu S, (2004) Signalling pathways in the molecular pathogenesis of ovarian granulosa cell tumours. Trends in Endocrinology & Metabolism 15: 122-128.
6. Fuller PJ, Chu S, Fikret S, Burger HG, (2002) Molecular pathogenesis of granulosa cell tumours. Molecular & Cellular Endocrinology 191: 89-96.
7. Cocquet J, Pailhoux E, Jaubert F, Servel N, Xia X, et al. (2002) Evolution and expression of FOXL2. Journal of medical genetics 39: 916-921.
8. Crisponi L, Deiana M, Loi A, Chiappe F, Uda M, et al. (2001) The putative forkhead transcription factor FOXL2 is mutated in blepharophimosis/ptosis/epicanthus inversus syndrome. Nature genetics 27: 159-166.
9. Schmidt D, Ovitt CE, Anlag K, Fehsenfeld S, Gredsted L, et al. (2004) The murine winged-helix transcription factor Foxl2 is required for granulosa cell differentiation and ovary maintenance. Development (Cambridge, England) 131: 933-942.
10. Uda M, Ottolenghi C, Crisponi L, Garcia JE, Deiana M, et al. (2004) Foxl2 disruption causes mouse ovarian failure by pervasive blockage of follicle development. Human molecular genetics 13: 1171-1181.
11. Harris SE, Chand AL, Winship IM, Gersak K, Aittomaki K, et al. (2002) Identification of novel mutations in FOXL2 associated with premature ovarian failure. Molecular Human Reproduction 8: 729-733.
12. Shah SP, Kobel M, Senz J, Morin RD, Clarke BA, et al. (2009) Mutation of FOXL2 in granulosa-cell tumors of the ovary. N Engl J Med 360: 2719-2729.
13. Jamieson S, Butzow R, Andersson N, Alexiadis M, Unkila-Kallio L, et al. (2010) The FOXL2 C134W mutation is characteristic of adult granulosa cell tumors of the ovary. Modern Pathology 23: 1477-1485.
14. Kim MS, Hur SY, Yoo NJ, Lee SH, (2010) Mutational analysis of FOXL2 codon 134 in granulosa cell tumour of ovary and other human cancers. J Pathol 221: 147-152.
15. D'Angelo E, Mozos A, Nakayama D, Espinosa I, Catasus L, et al. (2011) Prognostic significance of FOXL2 mutation and mRNA expression in adult and juvenile granulosa cell tumors of the ovary. Modern pathology: an official journal of the United States and Canadian Academy of Pathology, Inc 24: 1360-1367.
16. Schrader KA, Gorbatcheva B, Senz J, Heravi-Moussavi A, Melnyk N, et al. (2009) The specificity of the FOXL2 c.402C>G somatic mutation: a survey of solid tumors. PloS one 4: e7988.
17. Hes O, Vanecek T, Petersson F, Grossmann P, Hora M, et al. (2011) Mutational analysis (c.402C>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 19: 347-351.
18. Benayoun BA, Caburet S, Dipietromaria A, Georges A, D'Haene B, et al. (2010) Functional exploration of the adult ovarian granulosa cell tumor-associated somatic FOXL2 mutation p.Cys134Trp (c.402C>G). PloS one 5: e8789.
19. Kobel M, Gilks CB, Huntsman DG, (2009) Adult-type granulosa cell tumors and FOXL2 mutation. Cancer Res 69: 9160-9162.
20. Kim JH, Yoon S, Park M, Park HO, Ko JJ, et al. (2010) Differential apoptotic activities of wild-type FOXL2 and the adult-type granulosa cell tumor-associated mutant FOXL2 (C134W). Oncogene 30: 1653-1663.
21. Fleming NI, Knower KC, Lazarus KA, Fuller PJ, Simpson ER, et al. (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.
22. Nishi Y, Yanase T, Mu Y, Oba K, Ichino I, 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.
23. Zhang H, Vollmer M, De Geyter MD, Litzistorf Y, Ladewig A, et al. (2000) Characterization of an immortalized human granulosa cell line (COV434). Molecular Human Reproduction 6: 146-153.
24. Kalfa N, Fellous M, Boizet-Bonhoure B, Patte C, Duvillard P, et al. (2008) Aberrant expression of ovary determining gene FOXL2 in the testis and juvenile granulosa cell tumor in children. J Urol 180: 1810-1813.
25. Kalfa N, Philibert P, Patte C, Ecochard A, Duvillard P, et al. (2007) Extinction of FOXL2 expression in aggressive ovarian granulosa cell tumors in children. Fertil Steril 87: 896-901.
26. Ramakers C, Ruijter J, Deprez R, Moorman A, (2003) Assumption-free analysis of quantitative real-time polymerase chain reaction (PCR) data. Neuroscience Letters 339: 62-66.
27. Vandesompele J, De Preter K, Pattyn F, Poppe B, Van Roy N, et al. (2002) Accurate normalization of real-time quantitative RT-PCR data by geometric averaging of multiple internal control genes. Genome Biology 3: 1-12.
28. Parman C, Halling C (2006) affyQCReports: A package to generate QC reports for affymetrix array data.
29. Irizarry RA, Bolstad BM, Collin F, Cope LM, Hobbs B, et al. (2003) Summaries of Affymetrix GeneChip probe level data. Nucleic acids research 31: e15.
30. Smyth GK, (2004) Linear models and empirical bayes methods for assessing differential expression in microarray experiments. Stat Appl Genet Mol Biol 3: Article3.
31. Chang JT, Nevins JR, (2006) GATHER: a systems approach to interpreting genomic signatures. Bioinformatics 22: 2926-2933.
32. Araki H, Knapp C, Tsai P, Print C, (2012) GeneSetDB: a comprehensive meta-database, statistical and visualisation framework for gene set analysis. FEBS Open Bio 2: 76-82.
33. Garcia-Ortiz JE, Pelosi E, Omari S, Nedorezov T, Piao Y, et al. (2009) Foxl2 functions in sex determination and histogenesis throughout mouse ovary development. BMC developmental biology 9: 36.
34. Schlessinger D, Garcia-Ortiz JE, Forabosco A, Uda M, Crisponi L, et al. (2010) Determination and stability of gonadal sex. Journal of andrology 31: 16-25.
35. Uhlenhaut NH, Jakob S, Anlag K, Eisenberger T, Sekido R, et al. (2009) Somatic sex reprogramming of adult ovaries to testes by FOXL2 ablation. Cell 139: 1130-1142.
36. Veitia RA, (2010) FOXL2 versus SOX9: a lifelong "battle of the sexes". Bioessays 32: 375-380.
37. Benayoun BA, Georges AB, L'Hote D, Andersson N, Dipietromaria A, et al. (2011) Transcription factor FOXL2 protects granulosa cells from stress and delays cell cycle: role of its regulation by the SIRT1 deacetylase. Human molecular genetics 20: 1673-1686.
38. Batista F, Vaiman D, Dausset J, Fellous M, Veitia RA, (2007) Potential targets of FOXL2, a transcription factor involved in craniofacial and follicular development, identified by transcriptomics. Proceedings of the National Academy of Sciences of the United States of America 104: 3330-3335.
39. Escudero JM, 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. J Ovarian Res 3: 4.
40. Benayoun BA, Caburet S, Dipietromaria A, Bailly-Bechet M, Batista F, et al. (2008) The identification and characterization of a FOXL2 response element provides insights into the pathogenesis of mutant alleles. Human molecular genetics 17: 3118-3127.
41. Moumne L, Batista F, Benayoun BA, Nallathambi J, Fellous M, et al. (2008) The mutations and potential targets of the forkhead transcription factor FOXL2. Molecular and cellular endocrinology 282: 2-11.
42. Pisarska MD, Barlow G, Kuo FT, (2011) Minireview: roles of the forkhead transcription factor FOXL2 in granulosa cell biology and pathology. Endocrinology 152: 1199-1208.
43. Ellsworth BS, Burns AT, Escudero KW, Duval DL, Nelson SE, et al. (2003) 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. Molecular and cellular endocrinology 206: 93-111.
44. Corpuz PS, Lindaman LL, Mellon PL, Coss D, (2010) FoxL2 Is required for activin induction of the mouse and human follicle-stimulating hormone beta-subunit genes. Mol Endocrinol 24: 1037-1051.
45. Ayroles JF, Gibson G, (2006) Analysis of variance of microarray data. Methods in enzymology 411: 214-233.
46. Sansom SN, Griffiths DS, Faedo A, Kleinjan DJ, Ruan Y, et al. (2009) The level of the transcription factor Pax6 is essential for controlling the balance between neural stem cell self-renewal and neurogenesis. PLoS genetics 5: e1000511.
47. Schlessinger D, Garcia-Ortiz JE, Forabosco A, Uda M, Crisponi L, et al. (2009) Determination and stability of gonadal sex. Journal of andrology 31: 16-25.
48. Gittleman AM, Price AP, Coren C, Akhtar M, Donovan V, et al. (2003) Juvenile granulosa cell tumor. Clinical imaging 27: 221-224.
49. Arcellana-Panlilio MY, Egeler RM, Ujack E, Magliocco A, Stuart GC, et al. (2002) Evidence of a role for the INK4 family of cyclin-dependent kinase inhibitors in ovarian granulosa cell tumors. Genes, chromosomes & cancer 35: 176-181.
50. Rahimi RA, Leof EB, (2007) TGF-beta signaling: a tale of two responses. Journal of cellular biochemistry 102: 593-608.
51. Seoane J, (2006) Escaping from the TGFB antiproliferative control. Carcinogenesis 27: 2148-2156.
52. Wakefield L, Roberts A, (2002) TGFb signalling: positive and negative effects on tumourigenesis. Current Opinion in Genetics & Development 12: 22-29.