Adult ovarian granulosa cell tumor transcriptomics: Prevalence of FOXL2 target genes misregulation gives insights into the pathogenic mechanism of the p.Cys134Trp somatic mutation

Oncogene

Volumn 32, Issue 22, 2013, Pages 2739-2746

  Benayoun, B A ^a,b,f   Anttonen, M ^c,d   L'Hote D ^a,b   Bailly Bechet, M ^e   Andersson, N ^d   Heikinheimo, M ^d   Veitia, R A ^a,b  

^a INSTITUT JACQUES MONOD   (France)

^b UNIVERSITÉ PARIS DESCARTES   (France)

^c HELSINKI UNIVERSITY CENTRAL HOSPITAL   (Finland)

^d UNIVERSITY OF HELSINKI   (Finland)

^e UNIVERSITÉ DE LYON   (France)

^f STANFORD UNIVERSITY   (United States)

Author keywords

FOXL2; ovarian granulosa cell tumor; ovary; transcriptome

Indexed keywords

MEMBRANE PROTEIN; PROTEIN FOXL2; UNCLASSIFIED DRUG;

APOPTOSIS; ARTICLE; CANCER STAGING; CELL CYCLE M PHASE; CELL DEATH; CELL PROLIFERATION; CONTROLLED STUDY; DOWN REGULATION; FEMALE; GENE SEQUENCE; GENETIC ASSOCIATION; GRANULOSA CELL TUMOR; HETEROZYGOTE; HUMAN; HUMAN CELL; MALIGNANT TRANSFORMATION; MICROARRAY ANALYSIS; MOLECULAR DYNAMICS; MUTATIONAL ANALYSIS; NUCLEOTIDE SEQUENCE; OVARY CELL; PATHOGENESIS; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN TARGETING; SIGNAL TRANSDUCTION; SOMATIC MUTATION; TRANSCRIPTOMICS; WILD TYPE;

ADULT; AGED; CELL LINE, TUMOR; CELL PROLIFERATION; FEMALE; FORKHEAD TRANSCRIPTION FACTORS; GENE EXPRESSION PROFILING; GRANULOSA CELL TUMOR; GRANULOSA CELLS; HELA CELLS; HUMANS; MIDDLE AGED; MUTATION; OVARIAN NEOPLASMS; OVARY; TRANSCRIPTOME;

EID: 84879417843     PISSN: 09509232     EISSN: 14765594     Source Type: Journal    
DOI: 10.1038/onc.2012.298     Document Type: Article

References (40)

1. Pectasides D, Pectasides E, Psyrri A. Granulosa cell tumor of the ovary. Cancer Treat Rev 2008; 34: 1-12.
2. Schumer ST, Cannistra SA. Granulosa cell tumor of the ovary. J Clin Oncol 2003; 21: 1180-1189.
3. East N, Alobaid A, Goffin F, Ouallouche K, Gauthier P. Granulosa cell tumour: a recurrence 40 years after initial diagnosis. J Obstet Gynaecol Can 2005; 27: 363-364.
4. Kalfa N, Veitia RA, Benayoun BA, Boizet-Bonhoure B, Sultan C. The new molecular biology of granulosa cell tumors of the ovary. Genome Med 2009; 1: 81.
5. Benayoun BA, Caburet S, Dipietromaria A, Georges A, D'Haene B, Pandaranayaka PJ et al. Functional exploration of the adult ovarian granulosa cell tumor-associated somatic FOXL2 mutation p.Cys134Trp (c.402C4G). PLoS One 2010; 5: e8789.
6. Jamieson S, Butzow R, Andersson N, Alexiadis M, Unkila-Kallio L, Heikinheimo M et al. The FOXL2 C134W mutation is characteristic of adult granulosa cell tumors of the ovary. Mod Pathol 2010; 23: 1477-1485.
7. 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.
8. Schrader KA, Gorbatcheva B, Senz J, Heravi-Moussavi A, Melnyk N, Salamanca C et al. The specificity of the FOXL2 c.402C4G somatic mutation: a survey of solid tumors. PLoS One 2009; 4: e7988.
9. Shah SP, Kobel M, Senz J, Morin RD, Clarke BA, Wiegand KC et al. Mutation of FOXL2 in granulosa-cell tumors of the ovary. N Engl J Med 2009; 360: 2719-2729.
10. Crisponi L, Deiana M, Loi A, Chiappe F, Uda M, Amati P et al. The putative forkhead transcription factor FOXL2 is mutated in blepharophimosis/ ptosis/epicanthus inversus syndrome. Nat Genet 2001; 27: 159-166.
11. Cocquet J, Pailhoux E, Jaubert F, Servel N, Xia X, Pannetier M et al. Evolution and expression of FOXL2. J Med Genet. 2002; 39: 916-921.
12. Uhlenhaut NH, Jakob S, Anlag K, Eisenberger T, Sekido R, Kress J et al. Somatic sex reprogramming of adult ovaries to testes by FOXL2 ablation. Cell 2009; 139: 1130-1142.
13. Batista F, Vaiman D, Dausset J, Fellous M, Veitia RA. Potential targets of FOXL2, a transcription factor involved in craniofacial and follicular development, identified by transcriptomics. Proc Natl Acad Sci USA 2007; 104: 3330-3335.
14. Benayoun BA, Batista F, Auer J, Dipietromaria A, L'Hote D, De Baere E et al. 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: 632-644.
15. Benayoun BA, Georges AB, L'Hote D, Andersson N, Dipietromaria A, Todeschini AL et al. 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.
16. Lee K, Pisarska MD, Ko JJ, Kang Y, Yoon S, Ryou SM et al. Transcriptional factor FOXL2 interacts with DP103 and induces apoptosis. Biochem Biophys Res Commun 2005; 336: 876-881.
17. Kim JH, Yoon S, Park M, Park HO, Ko JJ, Lee K et al. Differential apoptotic activities of wild-type FOXL2 and the adult-type granulosa cell tumor-associated mutant FOXL2 (C134W). Oncogene 2011; 30: 1653-1663.
18. Benayoun BA, Kalfa N, Sultan C, Veitia RA. The forkhead factor FOXL2: a novel tumor suppressor? Biochim Biophys Acta 2010; 1805: 1-5.
19. 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.
20. Johnson WE, Li C, Rabinovic A. Adjusting batch effects in microarray expression data using empirical Bayes methods. Biostatistics 2007; 8: 118-127.
21. Nagaraja AK, Middlebrook BS, Rajanahally S, Myers M, Li Q, Matzuk MM et al. Defective gonadotropin-dependent ovarian folliculogenesis and granulosa cell gene expression in inhibin-deficient mice. Endocrinology 2010; 151: 4994-5006.
22. Tusher VG, Tibshirani R, Chu G. Significance analysis of microarrays applied to the ionizing radiation response. Proc Natl Acad Sci USA 2001; 98: 5116-5121.
23. Suzuki R, Shimodaira H. Pvclust: an R package for assessing the uncertainty in hierarchical clustering. Bioinformatics 2006; 22: 1540-1542.
24. Saldanha AJ. Java Treeview-extensible visualization of microarray data. Bioinfor-matics 2004; 20: 3246-3248.
25. Dennis Jr G, Sherman BT, Hosack DA, Yang J, Gao W, Lane HC et al. DAVID: database for annotation, visualization, and integrated discovery. Genome Biol. 2003; 4: P3.
26. Huangda W, Sherman BT, Lempicki RA. Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nat Protoc 2009; 4: 44-57.
27. Hanahan D, Weinberg RA. The hallmarks of cancer. Cell 2000; 100: 57-70.
28. Hanahan D, Weinberg RA. Hallmarks of cancer: the next generation. Cell 2011; 144: 646-674.
29. Kalfa N, Philibert P, Patte C, Ecochard A, Duvillard P, Baldet P et al. Extinction of FOXL2 expression in aggressive ovarian granulosa cell tumors in children. Fertil Steril 2007; 87: 896-901.
30. Pangas SA, Li X, Umans L, Zwijsen A, Huylebroeck D, Gutierrez C et al. Conditional deletion of Smad1 and Smad5 in somatic cells of male and female gonads leads to metastatic tumor development in mice. Mol Cell Biol 2008; 28: 248-257.
31. Eden E, Navon R, Steinfeld I, Lipson D, Yakhini Z. GOrilla: a tool for discovery and visualization of enriched GO terms in ranked gene lists. BMC Bioinformatics 2009; 10: 48.
32. Blount AL, Schmidt K, Justice NJ, Vale WW, Fischer WH, Bilezikjian LM. FoxL2 and Smad3 coordinately regulate follistatin gene transcription. J Biol Chem 2009; 284: 7631-7645.
33. Kyronlahti A, Kauppinen M, Lind E, Unkila-Kallio L, Butzow R, Klefstrom J et al. GATA4 protects granulosa cell tumors from TRAIL-induced apoptosis. Endocr Relat Cancer 2010; 17: 709-717.
34. Chen C, Grennan K, Badner J, Zhang D, Gershon E, Jin L et al. Removing batch effects in analysis of expression microarray data: an evaluation of six batch adjustment methods. PLoS One 2011; 6: e17238.
35. Heinz S, Benner C, Spann N, Bertolino E, Lin YC, Laslo P et al. Simple combinations of lineage-determining transcription factors prime cis-regulatory elements required for macrophage and B cell identities. Mol Cell 2010; 38: 576-589.
36. Moumne L, Dipietromaria A, Batista F, Kocer A, Fellous M, Pailhoux E et al. 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.
37. Kim HP, Roe JH, Chock PB, Yim MB. Transcriptional activation of the human manganese superoxide dismutase gene mediated by tetradecanoylphorbol acetate. J Biol Chem 1999; 274: 37455-37460.
38. Rishi AK, Sun RJ, Gao Y, Hsu CK, Gerald TM, Sheikh MS et al. Post-transcriptional regulation of the DNA damage-inducible gadd45 gene in human breast carcinoma cells exposed to a novel retinoid CD437. Nucleic Acids Res 1999; 27: 3111-3119.
39. Zhang H, Vollmer M, De Geyter M, Litzistorf Y, Ladewig A, Durrenberger M et al. Characterization of an immortalized human granulosa cell line (COV434). Mol Hum Reprod 2000; 6: 146-153.
40. Sambrook J, Russell DW. Molecular Cloning-A Laboratory Manual. 3 edn. Cold Spring Harbor Laboratory Press: New York, 2001.