FOXL2 in human endometrium: Hyperexpressed in endometriosis

Reproductive Sciences

Volumn 21, Issue 10, 2014, Pages 1249-1255

  Governini, Laura ^a   Carrarelli, Patrizia ^a   Rocha, Ana Luiza Lunardi ^b   Leo, Vincenzo De ^a   Luddi, Alice ^a   Arcuri, Felice ^a   Piomboni, Paola ^a   Chapron, Charles ^c   Bilezikjian, Louise M ^d   Petraglia, Felice ^a  

^a UNIVERSITY OF SIENA   (Italy)

^b FEDERAL UNIVERSITY OF MINAS GERAIS   (Brazil)

^c UNIVERSITÉ PARIS DESCARTES   (France)

^d SALK INSTITUTE FOR BIOLOGICAL STUDIES   (United States)

Author keywords

activin A; endometriosis; endometrium; FOXL2

Indexed keywords

ACTIVIN A; MESSENGER RNA; PROTEIN; PROTEIN FOXL2; SUMO 1 PROTEIN; UNCLASSIFIED DRUG; FORKHEAD TRANSCRIPTION FACTOR; FOXL2 PROTEIN, HUMAN;

ADULT; ARTICLE; CONTROLLED STUDY; ENDOMETRIOSIS; ENDOMETRIUM; FEMALE; GENE EXPRESSION; HUMAN; HYSTEROSCOPY; IMMUNOHISTOCHEMISTRY; MENSTRUAL CYCLE; NUCLEOTIDE SEQUENCE; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; REAL TIME POLYMERASE CHAIN REACTION; STROMA CELL; BIOSYNTHESIS; GENE EXPRESSION REGULATION; METABOLISM; PATHOLOGY;

ADULT; ENDOMETRIOSIS; ENDOMETRIUM; FEMALE; FORKHEAD TRANSCRIPTION FACTORS; GENE EXPRESSION REGULATION; HUMANS;

EID: 84905255410     PISSN: 19337191     EISSN: 19337205     Source Type: Journal    
DOI: 10.1177/1933719114522549     Document Type: Article

References (40)

1. Hannenhalli S, Kaestner KH. The evolution of Fox genes and their role in development and disease. Nat Rev Genet. 2009; 10 (4). 233-240
2. Grinius L, Kessler C, Schroeder J, Handwerger S. Forkhead transcription factor FOXO1A is critical for induction of human decidualization. J Endocrinol. 2006; 189 (1). 179-187
3. Takano M, Lu Z, Goto T, et al. Transcriptional cross talk between the forkhead transcription factor forkhead box O1A and the progesterone receptor coordinates cell cycle regulation and differentiation in human endometrial stromal cells. Mol Endocrinol. 2007; 21 (10). 2334-2349
4. Fu L, Girling JE, Rogers PA. Expression of Fox head protein 1 in human eutopic endometrium and endometriosis. Reprod Sci. 2008; 15 (3). 243-252
5. Christian M, Lam EW, Wilson MS, Brosens JJ. FOXO transcription factors and their role in disorders of the female reproductive tract. Curr Drug Targets. 2011; 12 (9). 1291-1302
6. Geiss-Friedlander R, Melchior F. Concepts in SUMO-1ylation: a decade on. Nat Rev Mol Cell Biol. 2007; 8 (12). 947-956
7. Ellsworth BS, Burns AT, Escudero KW, Duval DL, Nelson SE, Clay CM. 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 (1-2). 93-111
8. 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 (12). 7631-7645
9. Coss D, Mellon PL, Thackray VG. A FoxL in the Smad house: activin regulation of FSH. Trends Endocrinol Metab. 2010; 21 (9). 562-568
10. Schmidt D, Ovitt CE, Anlag K, et al. The murine winged-helix transcription factor Foxl2 is required for granulosa cell differentiation and ovary maintenance. Development. 2004; 131 (4). 933-942
11. Ottolenghi C, Omari S, Garcia-Ortiz JE, et al. Foxl2 is required for commitment to ovary differentiation. Hum Mol Genet. 2005; 14 (14). 2053-2062
12. Pisarska MD, Bae J, Klein C, Hsueh AJ. Forkhead l2 is expressed in the ovary and represses the promoter activity of the steroidogenic acute regulatory gene. Endocrinol. 2004; 145 (7). 3424-3433
13. Nelson LM, Covington SN, Rebar RW. An update: spontaneous premature ovarian failure is not an early menopause. Fertil Steril. 2005; 83 (5). 1327-1332
14. Jones MC, Fusi L, Higham JH, et al. Regulation of the SUMO-1 pathway sensitizes differentiating human endometrial stromal cells to progesterone. Proc Natl Acad Sci U S A. 2006; 103 (44). 16272-16277
15. Al-Sabbagh M, Lam EW, Brosens JJ. Mechanisms of endometrial progesterone resistance. Mol Cell Endocrinol. 2012; 358 (2). 208-215
16. Kuo FT, Bentsi-Barnes IK, Barlow GM, Bae J, Pisarska MD. Sumoylation of forkhead L2 by Ubc9 is required for its activity as a transcriptional repressor of the steroidogenic acute regulatory gene. Cell Signal. 2009; 21 (12). 1935-1944
17. Florio P, Severi FM, Luisi S, et al. Endometrial expression and secretion of activin A, but not follistatin, increase in the secretory phase of the menstrual cycle. J Soc Gynecol Invest. 2003; 10 (4). 237-243
18. Jones RL, Salamonsen LA, Findlay JK. Activin A promotes human endometrial stromal cell decidualization in vitro. J Clin Endocrinol Metab. 2002; 87 (8). 4001 4
19. Jones RL, Findlay JK, Farnworth PG, Robertson DM, Wallace E, Salamonsen LA. Activin A and inhibin A differentially regulate human uterine matrix metalloproteinases: potential interactions during decidualization and trophoblast invasion. Endocrinol. 2006; 147 (2). 724-732
20. Florio P, Gabbanini M, Borges LE, et al. Activins and related proteins in the establishment of pregnancy. Reprod Sci. 2010; 17 (4). 320-330
21. Reis FM, Di Blasio AM, Florio P, Ambrosini G, Di Loreto C, Petraglia F. Evidence for local production of inhibin A and activin A in patients with ovarian endometriosis. Fertil Steril. 2001; 75 (2). 367-373
22. Rocha AL, Carrarelli P, Novembri R, et al. Altered expression of activin, cripto, and follistatin in the endometrium of women with endometrioma. Fertil Steril. 2011; 95 (7). 2241-2246
23. Mangioni S, Viganò P, Florio P, et al. Effect of activin A on tumor necrosis factor-alpha/intercellular adhesion molecule-1 pathway in endometrial stromal cells. Eur J Obstet Gynecol Reprod Biol. 2005; 123 (2). 218-223
24. Rocha AL, Carrarelli P, Novembri R, et al. Activin A stimulates interleukin 8 and vascular endothelial growth factor release from cultured human endometrial stromal cells: possible implications for the pathogenesis of endometriosis. Reprod Sci. 2012; 19 (8). 832-838
25. Ferreira MC, Witz CA, Hammes LS, et al. Activin A increases invasiveness of endometrial cells in a in vitro model of human peritoneum. Mol Hum Reprod. 2008; 14 (5). 301-307
26. Eozenou C, Vitorino Carvalho A, Forde N, Giraud-Delville C, Gall L, Lonergan P. FOXL2 is regulated during the bovine estrous cycle and its expression in the endometrium is independent of conceptus-derived interferon Tau. Biol Reprod. 2012; 87 (2). 1-9
27. Honda H, Barrueto FF, Gogusev J, Im DD, Morin PJ. Serial analysis of gene expression reveals differential expression between endometriosis and normal endometrium. Possible roles for AXL and SHC1 in the pathogenesis of endometriosis. Reprod Biol Endocrinol. 2008; 6: 59
28. Borghese B, Mondon F, Noël JC, et al. Gene expression profile for ectopic versus eutopic endometrium provides new insights into endometriosis oncogenic potential. Mol Endocrinol. 2008; 22 (11). 2557-2562
29. Chung TK, Cheung TH, Huen NY, et al. Dysregulated microRNAs and their predicted targets associated with endometrioid endometrial adenocarcinoma in Hong Kong women. Int J Cancer. 2009; 124 (6). 1358-1365
30. Fertil Steril. 1985; 43 (3). 351-352
31. Noyes RW, Hertig AT, Rock J. Dating the endometrial biopsy. Am J Obstet Gynecol. 1975; 122 (2). 262-263
32. Marongiu M, Deiana M, Meloni A, et al. The forkhead transcription factor Foxl2 is SUMO-1ylated in both human and mouse: SUMO-1ylation affects its stability, localization, and activity. PLoS One. 2010; 5 (3). e9477
33. Kim JJ, Buzzio OL, Li S, Lu Z. Role of FOXO1A in the regulation of insulin-like growth factor-binding protein-1 in human endometrial cells: interaction with progesterone receptor. Biol Reprod. 2005; 73 (4). 833-839
34. Uhlenhaut NH, Jakob S, Anlag K, et al. Somatic sex reprogramming of adult ovaries to testes by FOXL2 ablation. Cell. 2009; 139 (6). 1130-1142
35. Shah SP, Köbel M, Senz J, et al. Mutation of FOXL2 in granulosa-cell tumors of the ovary. N Engl J Med. 2009; 360 (26). 2719-2729
36. Weigel D, Jürgens G, Küttner F, Seifert E, Jäckle H. The homeotic gene fork head encodes a nuclear protein and is expressed in the terminal regions of the Drosophila embryo. Cell. 1989; 57 (4). 645-658
37. Ghochani Y, Saini JK, Mellon PL, Thackray VG. FOXL2 is involved in the synergy between activin and progestins on the follicle-stimulating hormone-subunit promoter. Endocrinol. 2012; 153 (4). 2023-2033
38. Shazand K, Baban S, Prive C, et al. FOXO1 and c-jun transcription factors mRNA are modulated in endometriosis. Mol Hum Reprod. 2004; 10 (12). 871-877
39. Batista F, Vaiman D, Dausset J, Fellous M, Veitia R. Potential targets of FOXL2, a transcription factor involved in craniofacial and follicular development, identified by transcriptomics. PNAS. 2007; 104 (9). 3330-3335
40. Bukulmez O, Hardy DB, Carr BR, Word RN, Mendelson CR. Inflammatory status influences aromatase and steroid receptor expression in endometriosis. Endocrinol. 2008; 149 (3). 1190-1204