Granulosa cell tumor mutant FOXL2C134W suppresses GDF-9 and activin A-induced follistatin transcription in primary granulosa cells

Molecular and Cellular Endocrinology

Volumn 372, Issue 1-2, 2013, Pages 57-64

  McTavish, Kirsten J ^a   Nonis, David ^a   Hoang, Yvonne D ^a   Shimasaki, Shunichi ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Activin; Follistatin; FOXL2; GDF 9; Granulosa cell tumor; Ovary

Indexed keywords

ACTIVIN A; FOLLISTATIN; FORKHEAD TRANSCRIPTION FACTOR; GROWTH DIFFERENTIATION FACTOR 9; MUTANT PROTEIN; SMAD3 PROTEIN; TRANSCRIPTION FACTOR FOXL2; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CARCINOGENESIS; CONTROLLED STUDY; FEMALE; GRANULOSA CELL; GRANULOSA CELL TUMOR; HYPOPHYSIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; RAT; REGULATORY MECHANISM; TRANSCRIPTION INITIATION; TRANSCRIPTION REGULATION;

ACTIVINS; ANIMALS; CELLS, CULTURED; FEMALE; FOLLISTATIN; FORKHEAD TRANSCRIPTION FACTORS; GENE EXPRESSION REGULATION; GRANULOSA CELL TUMOR; GRANULOSA CELLS; GROWTH DIFFERENTIATION FACTOR 9; HUMANS; MUTATION, MISSENSE; PRIMARY CELL CULTURE; PROMOTER REGIONS, GENETIC; RATS; RATS, SPRAGUE-DAWLEY; RNA, MESSENGER; SMAD3 PROTEIN; TRANSCRIPTION, GENETIC; TRANSCRIPTIONAL ACTIVATION;

EID: 84877145477     PISSN: 03037207     EISSN: 18728057     Source Type: Journal    
DOI: 10.1016/j.mce.2013.03.021     Document Type: Article

References (64)

1. Benayoun B.A., Kalfa N., Sultan C., Veitia R.A. The forkhead factor FOXL2: a novel tumor suppressor?. Biochim. Biophys. Acta 2010, 1805:1-5.
2. Benayoun B.A., Caburet S., Dipietromaria A., Georges A., D'Haene B., Pandaranayaka P.J., L'Hote D., Todeschini A.L., Krishnaswamy S., Fellous M., De Baere E., Veitia R.A. Functional exploration of the adult ovarian granulosa cell tumor-associated somatic FOXL2 mutation p.Cys134Trp (c.402C>G). PLoS One 2010, 5:e8789.
3. Bentsi-Barnes I.K., Kuo F.T., Barlow G.M., Pisarska M.D. Human forkhead L2 represses key genes in granulosa cell differentiation including aromatase, P450scc, and cyclin D2. Fertil. Steril. 2010, 94:353-356.
4. Beysen D., Moumne L., Veitia R., Peters H., Leroy B.P., De Paepe A., De Baere E. Missense mutations in the forkhead domain of FOXL2 lead to subcellular mislocalization, protein aggregation and impaired transactivation. Hum. Mol. Genet. 2008, 17:2030-2038.
5. Beysen D., De Paepe A., De Baere E. FOXL2 mutations and genomic rearrangements in BPES. Hum. Mutat. 2009, 30:158-169.
6. Blount A.L., Vaughan J.M., Vale W.W., Bilezikjian L.M. A Smad-binding element in intron 1 participates in activin-dependent regulation of the follistatin gene. J. Biol. Chem. 2008, 283:7016-7026.
7. Blount A.L., Schmidt K., Justice N.J., Vale W.W., Fischer W.H., Bilezikjian L.M. FoxL2 and Smad3 coordinately regulate follistatin gene transcription. J. Biol. Chem. 2009, 284:7631-7645.
8. Cataldo N.A., Rabinovici J., Fujimoto V.Y., Jaffe R.B. Follistatin antagonizes the effects of activin-A on steroidogenesis in human luteinizing granulosa cells. J. Clin. Endocrinol. Metab. 1994, 79:272-277.
9. Cocquet J., Pailhoux E., Jaubert F., Servel N., Xia X., Pannetier M., De Baere E., Messiaen L., Cotinot C., Fellous M., Veitia R.A. Evolution and expression of FOXL2. J. Med. Genet. 2002, 39:916-921.
10. Cocquet J., De Baere E., Gareil M., Pannetier M., Xia X., Fellous M., Veitia R.A. Structure, evolution and expression of the FOXL2 transcription unit. Cytogenet. Genome Res. 2003, 101:206-211.
11. Corpuz P.S., Lindaman L.L., Mellon P.L., Coss D. FoxL2 Is required for activin induction of the mouse and human follicle-stimulating hormone beta-subunit genes. Mol. Endocrinol. 2010, 24:1037-1051.
12. 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., Pilia G. The putative forkhead transcription factor FOXL2 is mutated in blepharophimosis/ptosis/epicanthus inversus syndrome. Nat. Genet. 2001, 27:159-166.
13. De Baere E., Copelli S., Caburet S., Laissue P., Beysen D., Christin-Maitre S., Bouchard P., Veitia R., Fellous M. Premature ovarian failure and forkhead transcription factor FOXL2: blepharophimosis-ptosis-epicanthus inversus syndrome and ovarian dysfunction. Pediatr. Endocrinol. Rev. 2005, 2:653-660.
14. De Baere E., Fellous M., Veitia R.A. The transcription factor FOXL2 in ovarian function and dysfunction. Folia Histochem. Cytobiol. 2009, 47:S43-S49.
15. DePaolo L.V., Bicsak T.A., Erickson G.F., Shimasaki S., Ling N. Follistatin and activin: a potential intrinsic regulatory system within diverse tissues. Proc. Soc. Exp. Biol. Med. 1991, 198:500-512.
16. Dipietromaria A., Benayoun B.A., Todeschini A.L., Rivals I., Bazin C., Veitia R.A. Towards a functional classification of pathogenic FOXL2 mutations using transactivation reporter systems. Hum. Mol. Genet. 2009, 18:3324-3333.
17. Ellsworth B.S., Burns A.T., Escudero K.W., Duval D.L., Nelson S.E., 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. 2003, 206:93-111.
18. Ellsworth B.S., Egashira N., Haller J.L., Butts D.L., Cocquet J., Clay C.M., Osamura R.Y., Camper S.A. FOXL2 in the pituitary: molecular, genetic, and developmental analysis. Mol. Endocrinol. 2006, 20:2796-2805.
19. Erämaa M., Hildén K., Tuuri T., Ritvos O. Regulation of inhibin/activin subunit messenger ribonucleic acids (mRNAs) by activin A and expression of activin receptor mRNAs in cultured human granulosa-luteal cells. Endocrinology 1995, 136:4382-4389.
20. Fleming N.I., Knower K.C., Lazarus K.A., Fuller P.J., Simpson E.R., Clyne C.D. 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.
21. Fraser I.S., Shearman R.P., Smith A., Russell P. An association among blepharophimosis, resistant ovary syndrome, and true premature menopause. Fertil. Steril. 1988, 50:747-751.
22. Gershon R., Aviel-Ronen S., Korach J., Daniel-Carmi V., Avivi C., Bar-Ilan D., Barshack I., Meirow D., Ben-Baruch G., Cohen Y. FOXL2 C402G mutation detection using MALDI-TOF-MS in DNA extracted from Israeli granulosa cell tumors. Gynecol. Oncol. 2011, 122:580-584.
23. Hashimoto O., Kawasaki N., Tsuchida K., Shimasaki S., Hayakawa T., Sugino H. Difference between follistatin isoforms in the inhibition of activin signalling: activin neutralizing activity of follistatin isoforms is dependent on their affinity for activin. Cell Signal. 2000, 12:565-571.
24. Iemura S., Yamamoto T.S., Takagi C., Uchiyama H., Natsume T., Shimasaki S., Sugino H., Ueno N. Direct binding of follistatin to a complex of bone morphogenetic protein and its receptor inhibits ventral and epidermal cell fates in early Xenopus embryo. Proc. Natl. Acad. Sci. USA 1998, 95:9337-9342.
25. Inouye S., Guo Y., DePaolo L., Shimonaka M., Ling N., Shimasaki S. Recombinant expression of human follistatin with 315 and 288 amino acids: chemical and biological comparison with native porcine follistatin. Endocrinology 1991, 129:815-822.
26. Jamieson S., Butzow R., Andersson N., Alexiadis M., Unkila-Kallio L., Heikinheimo M., Fuller P.J., Anttonen M. The FOXL2 C134W mutation is characteristic of adult granulosa cell tumors of the ovary. Mod. Pathol. 2010, 23:1477-1485.
27. Kalfa N., Philibert P., Patte C., Ecochard A., Duvillard P., Baldet P., Jaubert F., Fellous M., Sultan C. Extinction of FOXL2 expression in aggressive ovarian granulosa cell tumors in children. Fertil. Steril. 2007, 87:896-901.
28. Kalfa N., Veitia R.A., Benayoun B.A., Boizet-Bonhoure B., Sultan C. The new molecular biology of granulosa cell tumors of the ovary. Genome Med. 2009, 1:81.
29. Kashimada K., Pelosi E., Chen H., Schlessinger D., Wilhelm D., Koopman P. FOXL2 and BMP2 act cooperatively to regulate follistatin gene expression during ovarian development. Endocrinology 2011, 152:272-280.
30. Knight P.G., Glister C. TGF-beta superfamily members and ovarian follicle development. Reproduction 2006, 132:191-206.
31. Kogawa K., Nakamura T., Sugino K., Takio K., Titani K., Sugino H. Activin-binding protein is present in pituitary. Endocrinology 1991, 128:1434-1440.
32. Kuo F.T., Fan K., Bentsi-Barnes I., Barlow G.M., Pisarska M.D. Mouse Forkhead L2 (FOXL2) maintains repression of FSH-dependent genes in the granulosa cell. Reproduction 2012.
33. Lamba P., Fortin J., Tran S., Wang Y., Bernard D.J. A novel role for the forkhead transcription factor FOXL2 in activin A-regulated follicle-stimulating hormone beta subunit transcription. Mol. Endocrinol. 2009, 23:1001-1013.
34. Lamba P., Wang Y., Tran S., Ouspenskaia T., Libasci V., Hebert T.E., Miller G.J., Bernard D.J. Activin A regulates porcine follicle-stimulating hormone beta-subunit transcription via cooperative actions of SMADs and FOXL2. Endocrinology 2010, 151:5456-5467.
35. Lee M.-J., Yang C.W., Jin D.C., Chang Y.S., Bang B.K., Kim Y.-S. Bone morphogenetic protein-7 inhibits constitutive and interleukin-1b-induced monocyte chemoattractant protein-1 expression in human mesangial cells: role for JNK/AP-1 pathway. J. Immunol. 2003, 170:2557-2563.
36. Loffler K.A., Zarkower D., Koopman P. Etiology of ovarian failure in blepharophimosis ptosis epicanthus inversus syndrome: FOXL2 is a conserved, early-acting gene in vertebrate ovarian development. Endocrinology 2003, 144:3237-3243.
37. Matzuk M.M., Kumar T.R., Vassalli A., Bickenbach J.R., Roop D.R., Jaenisch R., Bradley A. Functional analysis of activins during mammalian development. Nature 1995, 374:354-356.
38. Meduri G., Bachelot A., Duflos C., Bstandig B., Poirot C., Genestie C., Veitia R., De Baere E., Touraine P. FOXL2 mutations lead to different ovarian phenotypes in BPES patients: case report. Hum. Reprod. 2010, 25:235-243.
39. Miró F., Hillier S.G. Modulation of granulosa cell deoxyribonucleic acid synthesis and differentiation by activin. Endocrinology 1996, 137:464-468.
40. Nakamura T., Takio K., Eto Y., Shibai H., Titani K., Sugino H. Activin-binding protein from rat ovary is follistatin. Science 1990, 247:836-838.
41. Nakamura T., Hasegawa Y., Sugino K., Kogawa K., Titani K., Sugino H. Follistatin inhibits activin-induced differentiation of rat follicular granulosa cells in vitro. Biochim. Biophys. Acta 1992, 1135:103-109.
42. Nakatani A., Shimasaki S., DePaolo L.V., Erickson G.F., Ling N. Cyclic changes in follistatin messenger ribonucleic acid and its protein in the rat ovary during the estrous cycle. Endocrinology 1991, 129:603-611.
43. Nallathambi J., Moumne L., De Baere E., Beysen D., Usha K., Sundaresan P., Veitia R.A. 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, 121:107-112.
44. Otsuka F., Shimasaki S. A negative feedback system between oocyte bone morphogenetic protein 15 and granulosa cell kit ligand: its role in regulating granulosa cell mitosis. Proc. Natl. Acad. Sci. USA 2002, 99:8060-8065.
45. Otsuka F., Yao Z., Lee T.H., Yamamoto S., Erickson G.F., Shimasaki S. Bone morphogenetic protein-15: identification of target cells and biological functions. J. Biol. Chem. 2000, 275:39523-39528.
46. Otsuka F., Moore R.K., Iemura S.-I., Ueno N., Shimasaki S. Follistatin inhibits the function of the oocyte-derived factor BMP-15. Biochem. Biophys. Res. Commun. 2001, 289:961-966.
47. Pangas S.A., Matzuk M.M. Genetic models for transforming growth factor beta superfamily signaling in ovarian follicle development. Mol. Cell. Endocrinol. 2004, 225:83-91.
48. Pisarska M.D., Bae J., Klein C., Hsueh A.J. Forkhead l2 is expressed in the ovary and represses the promoter activity of the steroidogenic acute regulatory gene. Endocrinology 2004, 145:3424-3433.
49. Pisarska M.D., Barlow G., Kuo F.T. Minireview: roles of the forkhead transcription factor FOXL2 in granulosa cell biology and pathology. Endocrinology 2011.
50. Raile K., Stobbe H., Trobs R.B., 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, 153:353-358.
51. Roberts V.J., Barth S., El-Roeiy A., Yen S.S. Expression of inhibin/activin subunits and follistatin messenger ribonucleic acids and proteins in ovarian follicles and the corpus luteum during the human menstrual cycle. J. Clin. Endocrinol. Metab. 1993, 77:1402-1410.
52. Schmidt D., Ovitt C.E., Anlag K., Fehsenfeld S., Gredsted L., Treier A.C., Treier M. The murine winged-helix transcription factor Foxl2 is required for granulosa cell differentiation and ovary maintenance. Development 2004, 131:933-942.
53. Schneyer A.L., Rzucidlo D.A., Sluss P.M., Crowley W.F. Characterization of unique binding kinetics of follistatin and activin or inhibin in serum. Endocrinology 1994, 135:667-674.
54. Schumer S.T., Cannistra S.A. Granulosa cell tumor of the ovary. J. Clin. Oncol. 2003, 21:1180-1189.
55. 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., Huntsman D.G. Mutation of FOXL2 in granulosa-cell tumors of the ovary. New Engl. J. Med. 2009, 360:2719-2729.
56. Shimasaki S., Koga M., Esch F., Cooksey F., Mercado M., Koba A., Ueno N., Ying S.-Y., Ling N. Primary structure of the human follistatin precursor and its genomic organization. Proc. Natl. Acad. Sci., USA 1988, 85:4218-4222.
57. Shimasaki S., Koga M., Buscaglia M.L., Simmons D.M., Bicsak T.A., Ling N. Follistatin gene expression in the ovary and extragonadal tissues. Mol. Endocrinol. 1989, 3:651-659.
58. Shimasaki S., Moore R.K., Otsuka F., Erickson G.F. The bone morphogenetic protein system in mammalian reproduction. Endocrine Rev. 2004, 25:72-101.
59. Shimonaka M., Inouye S., Shimasaki S., Ling N. Follistatin binds to both activin and inhibin through the common ß-subunit. Endocrinology 1991, 128:3313-3315.
60. Woodruff T.K., D'Agostino J., Schwartz N.B., Mayo K.E. Dynamic changes in inhibin messenger RNAs in rat ovarian follicles during the reproductive cycle. Science 1988, 239:1296-1299.
61. Xiao S., Findlay J.K. Interaction between activin and follicle-stimulating hormone-suppressing protein and their mechanisms of action on cultured rat granulosa cells. Mol. Cell. Endocrinol. 1991, 79:99-107.
62. Xiao S., Robertson D.M., Findlay J.K. Effects of activin and follicle-stimulating hormone (FSH)-suppressing protein/follistatin on FSH receptors and differentiation of cultured rat granulosa cells. Endocrinology 1992, 131:1009-1016.
63. Xu J., Oakley J., McGee E.A. Stage-specific expression of Smad2 and Smad3 during folliculogenesis. Biol. Reprod. 2002, 66:1571-1578.
64. Yamashita H., ten Dijke P., Huylebroeck D., Sampath T.K., Andries M., Smith J.C., Heldin C.-H., Miyazono K. Osteogenic protein-1 binds to activin type II receptors and induces certain activin-like effects. J. Cell Biol. 1995, 130:217-226.