MicroRNA-133b stimulates ovarian estradiol synthesis by targeting Foxl2

FEBS Letters

Volumn 587, Issue 15, 2013, Pages 2474-2482

  Dai, Anyi ^a   Sun, Haixiang ^a   Fang, Ting ^a   Zhang, Qun ^a   Wu, Shaogen ^a   Jiang, Yue ^a   Ding, Lijun ^a   Yan, Guijun ^a   Hu, Yali ^a  

^a THE AFFILIATED DRUM TOWER HOSPITAL OF NANJING UNIVERSITY MEDICAL SCHOOL   (China)

Author keywords

CYP19A1; Estrogen; Foxl2; Granulosa cell; miR 133b; StAR

Indexed keywords

AROMATASE; ESTRADIOL; ESTROGEN; FOLLITROPIN; FORKHEAD TRANSCRIPTION FACTOR; LUCIFERASE; MESSENGER RNA; MICRORNA; MICRORNA 133B; STEROIDOGENIC ACUTE REGULATORY PROTEIN; TRANSCRIPTION FACTOR FOXL2; UNCLASSIFIED DRUG;

3' UNTRANSLATED REGION; ANIMAL CELL; ARTICLE; CONTROLLED STUDY; DOWN REGULATION; ENZYME ASSAY; ESTROGEN RELEASE; ESTROGEN SYNTHESIS; FEMALE; GENE OVEREXPRESSION; GENE TARGETING; GRANULOSA CELL; HUMAN; HUMAN CELL; INHIBITION KINETICS; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN TARGETING; STEROIDOGENESIS; TRANSCRIPTION REGULATION;

3′ UNTRANSLATED REGION; 3′UTR; ACTIVIN RECEPTOR TYPEIB; ACTIVIN RECEPTOR TYPEIIA; ACVRIB; ACVRIIA; ADENOSINE-3′:5′-MONOPHOSPHATE; CAMP; CAMP RESPONSE ELEMENT BINDING PROTEIN; CHIP; CHROMATIN IMMUNOPRECIPITATION; CREB; CYP; CYP19A1; CYTOCHROME P450; ERK; ESTROGEN; EXTRACELLULAR REGULATED KINASE; FOLLICLE-STIMULATING HORMONE; FORKHEAD L2; FOXL2; FSH; GRANULOSA CELL; LH; LUTEINIZING HORMONE; MAPK; MGCS; MICRORNA-133B; MIR-133B; MITOGEN-ACTIVATED PROTEIN KINASE; MOUSE GRANULOSA CELLS; PHOSPHOINOSITIDE 3-KINASE; PI3K; PKA; POF; PREMATURE OVARIAN FAILURE; PROTEIN KINASE A; RBMS1; RNA BINDING MOTIF, SINGLE STRANDED INTERACTING PROTEIN 1; STAR; STEROIDOGENIC ACUTE REGULATORY PROTEIN;

3' UNTRANSLATED REGIONS; ANIMALS; BASE SEQUENCE; CYTOCHROME P-450 ENZYME SYSTEM; DNA PRIMERS; ESTRADIOL; FEMALE; FOLLICLE STIMULATING HORMONE; FORKHEAD TRANSCRIPTION FACTORS; HUMANS; MICE; MICE, INBRED ICR; MICRORNAS; OVARY; PHOSPHOPROTEINS; PROMOTER REGIONS, GENETIC; REAL-TIME POLYMERASE CHAIN REACTION;

EID: 84880697003     PISSN: 00145793     EISSN: 18733468     Source Type: Journal    
DOI: 10.1016/j.febslet.2013.06.023     Document Type: Article

References (41)

1. M.M. Matzuk, and D.J. Lamb The biology of infertility: research advances and clinical challenges Nat. Med. 14 11 2008 1197 1213
2. T. Laml, I. Schulz-Lobmeyr, A. Obruca, J.C. Huber, and B.W. Hartmann Premature ovarian failure: etiology and prospects Gynecol. Endocrinol. 14 4 2000 292 302
3. N.H. Uhlenhaut, and M. Treier Forkhead transcription factors in ovarian function Reproduction 142 4 2011 489 495
4. M. Uda, C. Ottolenghi, L. Crisponi, J.E. Garcia, M. Deiana, W. Kimber, A. Forabosco, A. Cao, D. Schlessinger, and G. Pilia Foxl2 disruption causes mouse ovarian failure by pervasive blockage of follicle development Hum. Mol. Genet. 13 11 2004 1171 1181
5. M.D. Pisarska, G. Barlow, and F.T. Kuo Minireview: roles of the forkhead transcription factor FOXL2 in granulosa cell biology and pathology Endocrincology 152 4 2011 1199 1208
6. D. Schmidt, C.E. Ovitt, K. Anlag, S. Fehsenfeld, L. Gredsted, A.C. Treier, and M. Treier The murine winged-helix transcription factor Foxl2 is required for granulosa cell differentiation and ovary maintenance Development 131 4 2004 933 942
7. S. Caburet, A. Georges, D. L'Hôte, A.L. Todeschini, B.A. Benayoun, and R.A. Veitia The transcription factor FOXL2: at the crossroads of ovarian physiology and pathology Mol. Cell. Endocrinol. 356 1-2 2012 55 64
8. D.M. Stocco StAR protein and the regulation of steroid hormonebiosynthesis Annu. Rev. Physiol. 63 2001 193 213
9. V. Ambros The functions of animal microRNAs Nature 431 7006 2004 350 355
10. D.P. Bartel MicroRNA: genomics, biogenesis, mechanism, and function Cell 116 2 2004 281 297
11. L. Lei, S. Jin, G. Gonzalez, R.R. Behringer, and T.K. Woodruff The regulatory role of Dicer in folliculogenesis in mice Mol. Cell. Endocrinol. 315 1-2 2010 63 73
12. J. Baley, and J. Li MicroRNAs and ovarian function J. Ovarian Res. 5 2012 8
13. G. Yan, L. Zhang, T. Fang, Q. Zhang, S. Wu, Y. Jiang, H. Sun, and Y. Hu MicroRNA-145 suppresses mouse granulosa cell proliferation by targeting activin receptor 1B FEBS Lett. 586 19 2012 3263 3270
14. Q. Zhang, H. Sun, Y. Jiang, L. Ding, S. Wu, T. Fang, G. Yan, and Y. Hu MicroRNA-181a suppresses mouse granulosa cell proliferation by targeting activin receptor IIA PLoS One 8 3 2013 e59667
15. M. Yin, M. Lü, G. Yao, H. Tian, J. Lian, L. Liu, M. Liang, Y. Wang, and F. Sun Transactivation of microRNA-383 by steroidogenic factor-1 promotes estradiol release from mouse ovarian granulosa cells by targeting RBMS1 Mol. Endocrinol. 26 7 2012 1129 1143
16. S. Xu, K. Linher-Melville, B.B. Yang, D. Wu, and J. Li Micro-RNA378 (miR-378) regulates ovarian estradiol production by targeting aromatase Endocrinology 152 10 2011 3941 3951
17. G. Yao, M. Yin, J. Lian, H. Tian, L. Liu, X. Li, and F. Sun MicroRNA-224 is involved in transforming growth factor-beta-mediated mouse granulosa cell proliferation and granulosa cell function by targeting Smad4 Mol. Endocrinol. 24 3 2010 540 551
18. J.P. Patron, A. Fendler, M. Bild, U. Jung, H. Müller, Arntzen, M.ø, C. Piso, C. Stephan, B. Thiede, H.J. Mollenkopf, K. Jung, S.H. Kaufmann, and J. Schreiber MiR-133b targets antiapoptotic genes and enhances death receptor-induced apoptosis PLoS One 7 4 2012 e35345
19. F.M. Sanchez-Simon, X.X. Zhang, H.H. Loh, P.Y. Law, and R.E. Rodriguez Morphine regulates dopaminergic neuron differentiation via miR-133b Mol. Pharmacol. 78 5 2010 935 942
20. J.L. Kipp, and K.E. Mayo Use of reporter genes to study the activity of promoters in ovarian granulosa cells Methods Mol. Biol. 590 2009 177 193
21. Y. Nish, T. Yanase, Y. Mu, K. Oba, I. Ichino, M. Saito, M. Nomura, C. Mukasa, T. Okabe, K. Goto, R. Takayanagi, Y. Kashimura, M. Haji, and H. Nawata Establishment and characterization of a steroidogenic human granulosa-like tumor cell line, KGN, that expresses functional follicle-stimulating hormone receptor Endocrinology 142 1 2001 437 445
22. K.J. Livak, and T.D. Schmittgen Analysis of relative gene expression data using real-time quantitative PCR and the 2(-ΔΔC(T)) method Methods 25 4 2001 402 408
23. G. Yan, B. You, S.P. Chen, J.K. Liao, and J. Sun Tumor necrosis factor-alpha downregulates endothelial nitric oxide synthase mRNA stability via translation elongation factor 1-alpha 1 Circ. Res. 103 6 2008 591 597
24. A. Dai, G. Yan, Q. He, Y. Jiang, Q. Zhang, T. Fang, L. Ding, J. Sun, H. Sun, and Y. Hu Orphan nuclear receptor Nur77 regulates androgen receptor gene expression in mouse ovary PLoS One 7 6 2012 e39950
25. F.T. Kuo, K. Fan, I. Bentsi-Barnes, G.M. Barlow, and M.D. Pisarska Mouse forkhead L2 maintains repression of FSH-dependent genes in the granulosa cell Reproduction 144 4 2012 485 494
26. I.K. Bentsi-Barnes, F.T. Kuo, G.M. Barlow, and M.D. Pisarska Human forkhead L2 represses key genes in granulosa cell differentiation including aromatase, P450scc, and cyclin D2 Fertil. Steril. 94 1 2010 353 356
27. N. Yao, B.Q. Yang, Y. Liu, X.Y. Tan, C.L. Lu, X.H. Yuan, and X. Ma Follicle-stimulating hormone regulation of microRNA expression on progesterone production in cultured rat granulosa cells Endocrine 38 2 2010 158 166
28. R. Sasson, A. Dantes, K. Tajima, and A. Amsterdam Novel genes modulated by FSH in normal and immortalized FSH-responsive cells: new insights into the mechanism of FSH action FASEB J. 17 10 2003 1256 1266
29. A. Ulloa-Aguirre, T. Zariñán, A.M. Pasapera, P. Casas-González, and J.A. Dias Multiple facets of follicle-stimulating hormone receptor function Endocrine 32 3 2007 251 263
30. N.H. Uhlenhaut, and M. Treier Foxl2 function in ovarian development Mol. Genet. Metab. 88 3 2006 225 234
31. J. Cocquet, E. De Baere, M. Gareil, M. Pannetier, X. Xia, M. Fellous, and R.A. Veitia Structure, evolution and expression of the FOXL2 transcription unit Cytogenet. Genome Res. 101 3-4 2003 206 211
32. F.T. Kuo, I.K. Bentsi-Barnes, G.M. Barlow, and M.D. Pisarska Mutant forkhead L2 (FOXL2) proteins associated with premature ovarian failure (POF) dimerize with wild-type FOXL2, leading to altered regulation of genes associated with granulosa cell differentiation Endocrinology 152 10 2011 3917 3929
33. B.A. Benayoun, A.B. Georges, D. L'Hôte, N. Andersson, A. Dipietromaria, A.L. Todeschini, S. Caburet, C. Bazin, M. Anttonen, and R.A. Veitia Transcription factor FOXL2 protects granulosa cells from stress and delays cell cycle: role of its regulation by the SIRT1 deacetylase Hum. Mol. Genet. 20 9 2011 1673 1686
34. M.D. Pisarska, J. Bae, C. Klein, and A.J. Hsueh Forkhead L2 is expressed in the ovary and represses the promoter activity of the steroidogenic acute regulatory gene Endocrinology 145 7 2004 3424 3433
35. Y. Tsuchiya, M. Nakajima, and T. Yokoi Cytochrome P450-mediated metabolism of estrogens and its regulation in human Cancer Lett. 227 2 2005 115 124
36. S.G. Hillier, L.E. Reichert Jr., and E.V. Van Hall Control of preovulatory follicular estrogen biosynthesis in the human ovary J. Clin. Endocrinol. Metab. 52 5 1981 847 856
37. C.S. Rosenfeld, J.S. Wagner, R.M. Roberts, and D.B. Lubahn Intraovarian actions of oestrogen Reproduction 122 2 2001 215 226
38. M. Mihm, E.J. Austin, T.E. Good, J.L. Ireland, P.G. Knight, J.F. Roche, and J.J. Ireland Identification of potential intrafollicular factors involved in selection of dominant follicles in heifers Biol. Reprod. 63 3 2000 811 819
39. S.M. Quirk, R.G. Cowan, and R.M. Harman The susceptibility of granulosa cells to apoptosis is influenced by oestradiol and the cell cycle J. Endocrinol. 189 3 2006 441 453
40. Y. Chen, K. Breen, and M.E. Pepling Estrogen can signal through multiple pathways to regulate oocyte cyst breakdown and primordial follicle assembly in the neonatal mouse ovary J. Endocrinol. 202 3 2009 407 417
41. A.E. Drummond The role of steroids in follicular growth Reprod. Biol. Endocrinol. 4 2006 16