Involvement of miRNAs in ovarian follicular and luteal development

Journal of Endocrinology

Volumn 215, Issue 3, 2012, Pages 323-334

  Donadeu, F X ^a   Schauer, S N ^a   Sontakke, S D ^a  

^a UNIVERSITY OF EDINBURGH   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

EXPORTIN 5; MICRORNA; MIR 224; MIR 378; MIR 383; RIBONUCLEOPROTEIN; UNCLASSIFIED DRUG;

3' UNTRANSLATED REGION; CELL SURVIVAL; CORPUS LUTEUM; COW; CYTOLOGY; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; HUMAN; IN VITRO STUDY; NONHUMAN; OVARY FOLLICLE DEVELOPMENT; OVULATION; PRIORITY JOURNAL; REVIEW; SEQUENCE ANALYSIS; SHEEP; STEROIDOGENESIS; SWINE; TRANSGENIC MOUSE;

ANIMALS; CORPUS LUTEUM; FEMALE; HUMANS; MICRORNAS; OVARIAN FOLLICLE;

EID: 84872172372     PISSN: 00220795     EISSN: 14796805     Source Type: Journal    
DOI: 10.1530/JOE-12-0252     Document Type: Review

References (77)

1. AgcaC, Ries JE,Kolath SJ, KimJ-H, Forrester LJ,Antoniou E,Whitworth KM, MathialaganN, Springer GK, Prather RS et al. 2006 Luteinization of porcine preovulatory follicles leads to systematic changes in follicular gene expression. Reproduction 132 133-145. (doi:10.1530/rep.1.01163)
2. AhnHW, MorinRD, Zhao H, Harris RA, CoarfaC, Chen ZJ,Milosavljevic A, MarraMA & Rajkovic A 2010 MicroRNA transcriptome in the newborn mouse ovaries determined by massive parallel sequencing. Molecular Human Reproduction 16 463-471. (doi:10.1093/molehr/gaq017)
3. Ambros V 2004 The functions of animal microRNAs. Nature 431 350-355. (doi:10.1038/nature02871)
4. Berezikov E 2011 Evolution of microRNA diversity and regulation in animals. Nature Reviews. Genetics 12 846-860. (doi:10.1038/nrg3079)
5. Bogan RL, Murphy MJ & Hennebold JD 2009 Dynamic changes in gene expression that occur during the period of spontaneous functional regression in the rhesus macaque corpus luteum. Endocrinology 150 1521-1529. (doi:10.1210/en.2008-1201)
6. Campbell BK, Souza C, Gong J,Webb R, KendallN, Marsters P, Robinson G, Mitchell A, Telfer EE & Baird DT 2003 Domestic ruminants as models for the elucidation of the mechanisms controlling ovarian follicle development in humans. Reproduction. Supplement 61 429-443.
7. Caporali A, Meloni M, Vollenkle C, Bonci D, Sala-Newby GB, Addis R, Spinetti G, Losa S, Masson R, Baker AH et al. 2011 Deregulation of microRNA-503 contributes to diabetes mellitus-induced impairment of endothelial function and reparative angiogenesis after limb ischemia. Circulation 123 282-291. (doi:10.1161/CIRCULATIONAHA.110. 952325)
8. Carletti MZ, Fiedler SD & Christenson LK 2010 MicroRNA 21 blocks apoptosis in mouse periovulatory granulosa cells. Biology of Reproduction 83 286-295. (doi:10.1095/biolreprod.109.081448)
9. Cheng G, Sun S, Wang Z & Jin S 2012 Investigation of the interaction between the MIR-503 and CD40 genes in irradiated U937 cells. Radiation Oncology 7 38. (doi:10.1186/1748-717X-7-38)
10. Chi SW, Zang JB, Mele A & Darnell RB 2009 Argonaute HITS-CLIP decodes microRNA-mRNA interaction maps. Nature 460 479-486.
11. Cordes KR, Sheehy NT, White MP, Berry EC, Morton SU, Muth AN, Lee TH, Miano JM, Ivey KN & Srivastava D 2009 miR-145 and miR-143 regulate smooth muscle cell fate and plasticity. Nature 460 705-710.
12. Croce CM 2009 Causes and consequences of microRNA dysregulation in cancer. Nature Reviews. Genetics 10 704-714. (doi:10.1038/nrg2634)
13. Dammer EB & Sewer MB 2008 Phosphorylation of CtBP1 by cAMPdependent protein kinase modulates induction of CYP17 by stimulating partnering of CtBP1 and 2. Journal of Biological Chemistry 283 6925-6934. (doi:10.1074/jbc.M708432200)
14. Donadeu FX, Esteves CL, Doyle LK, Walker CA, Schauer SN & Diaz CA 2011 Phospholipase Cbeta3 mediates LH-induced granulosa cell differentiation. Endocrinology 152 2857-2869. (doi:10.1210/en.2010-1298)
15. Espey LL & Richards JS 2002 Temporal and spatial patterns of ovarian gene transcription following an ovulatory dose of gonadotropin in the rat. Biology of Reproduction 67 1662-1670. (doi:10.1095/biolreprod.102.005173)
16. Evans A, Ireland J, Winn M, Lonergan P, Smith G, Coussens P & Ireland J 2004 Identification of genes involved in apoptosis and dominant follicle development during follicular waves in cattle. Biology of Reproduction 70 1475-1484. (doi:10.1095/biolreprod.103.025114)
17. Fiedler SD, Carletti MZ, Hong X & Christenson LK 2008 Hormonal regulation of MicroRNA expression in periovulatory mouse mural granulosa cells. Biology of Reproduction 79 1030-1037. (doi:10.1095/ biolreprod.108.069690)
18. Friedman RC, Farh KK, Burge CB & Bartel DP 2009 Most mammalian mRNAs are conserved targets of microRNAs. Genome Research 19 92-105. (doi:10.1101/gr.082701.108)
19. Gonzalez G & Behringer RR 2009 Dicer is required for female reproductive tract development and fertility in the mouse. Molecular Reproduction and Development 76 678-688. (doi:10.1002/mrd.21010)
20. Guo H, Ingolia NT,Weissman JS & Bartel DP 2010 Mammalian microRNAs predominantly act to decrease target mRNA levels. Nature 466 835-840. (doi:10.1038/nature09267)
21. Gutierrez CCampbell B & Webb R 1997 Development of a long-term bovine granulosa cell culture system: induction and maintenance of estradiol production, response to follicle-stimulating hormone, and morphological characteristics. Biology of Reproduction 56 608-616. (doi:10.1095/biolreprod56.3.608)
22. HamelM, Dufort I, Robert C, Gravel C, Leveille MC, Leader A & Sirard MA 2008 Identification of differentially expressed markers in human follicular cells associated with competent oocytes. Human Reproduction 23 1118-1127. (doi:10.1093/humrep/den048)
23. Hawkins SM, Buchold GM & Matzuk MM 2011 Minireview: the roles of small RNA pathways in reproductive medicine. Molecular Endocrinology 25 1257-1279. (doi:10.1210/me.2011-0099)
24. Hong X, Luense LJ, McGinnis LK, Nothnick WB & Christenson LK 2008 Dicer1 is essential for female fertility and normal development of the female reproductive system. Endocrinology 149 6207-6212. (doi:10.1210/ en.2008-0294)
25. Hossain MM, Ghanem N, Hoelker M, Rings F, Phatsara C, Tholen E, Schellander K & Tesfaye D 2009 Identification and characterization of miRNAs expressed in the bovine ovary. BMC Genomics 10 443. (doi:10.1186/1471-2164-10-443)
26. Huang J, Ju Z, Li Q, Hou Q,Wang C, Li J, Li R,Wang L, Sun T, Hang S et al. 2011 Solexa sequencing of novel and differentially expressed microRNAs in testicular and ovarian tissues in Holstein cattle. International Journal of Biological Sciences 7 1016-1026. (doi:10.7150/ijbs.7.1016)
27. Huntzinger E & Izaurralde E 2011 Gene silencing by microRNAs: contributions of translational repression and mRNA decay. Nature Reviews. Genetics 12 99-110. (doi:10.1038/nrg2936)
28. Kozomara A & Griffiths-Jones S 2011 miRBase: integrating microRNA annotation and deep-sequencing data. Nucleic Acids Research 39 D152-D157. (doi:10.1093/nar/gkq1027)
29. Landgraf P, Rusu M, Sheridan R, Sewer A, Iovino N, Aravin A, Pfeffer S, Rice A, Kamphorst AO, Landthaler M et al. 2007 A mammalian microRNA expression atlas based on small RNA library sequencing. Cell 129 1401-1414. (doi:10.1016/j.cell.2007.04.040)
30. Laterza OF, Lim L, Garrett-Engele PW, Vlasakova K, Muniappa N, Tanaka WK, Johnson JM, Sina JF, Fare TL, Sistare FD et al. 2009 Plasma microRNAs as sensitive and specific biomarkers of tissue injury. Clinical Chemistry 55 1977-1983. (doi:10.1373/clinchem.2009.131797)
31. Lei L, Jin S, Gonzalez G, Behringer RR &Woodruff TK 2010 The regulatory role of Dicer in folliculogenesis in mice. Molecular and Cellular Endocrinology 315 63-73. (doi:10.1016/j.mce.2009.09.021)
32. Li M, Liu Y,Wang T, Guan J, Luo Z, Chen H,Wang X, Chen L, Ma J, Mu Z et al. 2011 Repertoire of porcine microRNAs in adult ovary and testis by deep sequencing. International Journal of Biological Sciences 7 1045-1055. (doi:10.7150/ijbs.7.1045)
33. Lin F, Li R, Pan ZX, Zhou B, Yu de B,Wang XG, Ma XS, Han J, Shen M & Liu HL 2012 miR-26b promotes granulosa cell apoptosis by targeting ATM during follicular atresia in porcine ovary. PLoS ONE 7 e38640. (doi:10.1371/journal.pone.0038640)
34. Liu J, Park E-S & Jo M 2009 Runt-related transcription factor 1 regulates luteinized hormone-induced prostaglandin-endoperoxide synthase 2 expression in rat periovulatory granulosa cells. Endocrinology 150 3291-3300. (doi:10.1210/en.2008-1527)
35. Liu LZ, Li C, Chen Q, Jing Y, Carpenter R, Jiang Y, Kung HF, Lai L & Jiang BH 2011 MiR-21 induced angiogenesis through AKT and ERK activation and HIF-1a expression. PLoS ONE 6 e19139. (doi:10.1371/ journal.pone.0019139)
36. Ma T, Jiang H, Gao Y, Zhao Y, Dai L, Xiong Q, Xu Y, Zhao Z & Zhang J 2011 Microarray analysis of differentially expressed microRNAs in nonregressed and regressed bovine corpus luteum tissue; microRNA-378 may suppress luteal cell apoptosis by targeting the interferon gamma receptor 1 gene. Journal of Applied Genetics 52 481-486. (doi:10.1007/s13353-011-0055-z)
37. McBride D, Carre W, Sontakke S, Hogg CO, Law AS, Donadeu FX & Clinton M 2012 Identification of miRNAs associated with the follicular-luteal transition in the ruminant ovary. Reproduction 144 221-233. (doi:10.1530/REP-12-0025)
38. Miles JR, McDaneld TG, Wiedmann RT, Cushman RA, Echternkamp SE, Vallet JL & Smith TP 2012 MicroRNA expression profile in bovine cumulus-oocyte complexes: possible role of let-7 and miR-106a in the development of bovine oocytes. Animal Reproduction Science 130 16-26. (doi:10.1016/j.anireprosci.2011.12.021)
39. Mishima T, Takizawa T, Luo S-S, Ishibashi O, Kawahigashi Y, Mizuguchi Y, Ishikawa T, Mori M, Kanda T, Goto T et al. 2008 MicroRNA (miRNA) cloning analysis reveals sex differences in miRNA expression profiles between adult mouse testis and ovary. Reproduction 136 811-822. (doi:10.1530/REP-08-0349)
40. Muramatsu F, Kidoya H, Naito H, Sakimoto S & Takakura N 2012 microRNA-125b inhibits tube formation of blood vessels through translational suppression of VE-cadherin. Oncogene. In press. (doi:10.1038/ onc.2012.68)
41. Murphy BD 2000 Models of luteinization. Biology of Reproduction 63 2-11. (doi:10.1095/biolreprod63.1.2)
42. Nagaraja AK, Andreu-Vieyra C, Franco HL,Ma L, Chen R, Han DY, Zhu H, Agno JE, Gunaratne PH, DeMayo FJ et al. 2008 Deletion of Dicer in somatic cells of the female reproductive tract causes sterility. Molecular Endocrinology 22 2336-2352. (doi:10.1210/me.2008-0142)
43. Otsuka M, Zheng M, Hayashi M, Lee JD, Yoshino O, Lin S & Han J 2008 Impaired microRNA processing causes corpus luteum insufficiency and infertility in mice. Journal of Clinical Investigation 118 1944-1954. (doi:10.1172/JCI33680)
44. Park CY, Choi YS & McManus MT 2010 Analysis of microRNA knockouts in mice. Human Molecular Genetics 19 R169-R175. (doi:10.1093/hmg/ ddq367)
45. Parker KL & Schimmer BP 1997 Steroidogenic factor 1: a key determinant of endocrine development and function. Endocrine Reviews 18 361-377. (doi:10.1210/er.18.3.361)
46. Pasquinelli AE 2012 MicroRNAs and their targets: recognition, regulation and an emerging reciprocal relationship. Nature Reviews. Genetics 13 271-282.
47. Patel SS, Beshay VE, Escobar JC, Suzuki T & Carr BR 2009 Molecular mechanism for repression of 17a-hydroxylase expression and androstenedione production in granulosa cells. Journal of Clinical Endocrinology and Metabolism 94 5163-5168. (doi:10.1210/jc.2009-1341)
48. Pfeifer A & Lehmann H 2010 Pharmacological potential of RNAi -focus on miRNA. Pharmacology & Therapeutics 126 217-227. (doi:10.1016/ j.pharmthera.2010.03.006)
49. 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. (doi:10.1210/en.2010-1041)
50. Ro S, Song R, Park C, Zheng H, Sanders KM & Yan W 2007 Cloning and expression profiling of small RNAs expressed in the mouse ovary. RNA 13 2366-2380. (doi:10.1261/rna.754207)
51. Roy S, Khanna S, Hussain S-RA, Biswas S, Azad A, Rink C, Gnyawali S, Shilo S, Nuovo GJ & Sen CK 2009 MicroRNA expression in response to murine myocardial infarction: miR-21 regulates fibroblast metalloprotease-2 via phosphatase and tensin homologue. Cardiovascular Research 82 21-29. (doi:10.1093/cvr/cvp015)
52. Ruby JG, Jan CH & Bartel DP 2007 Intronic microRNA precursors that bypass Drosha processing. Nature 448 83-86. (doi:10.1038/nature05983)
53. Sayed D & Abdellatif M 2011 MicroRNAs in development and disease. Physiological Reviews 91 827-887. (doi:10.1152/physrev.00006.2010)
54. Schwarzenbach H, Hoon DS & Pantel K 2011 Cell-free nucleic acids as biomarkers in cancer patients. Nature Reviews. Cancer 11 426-437. (doi:10.1038/nrc3066)
55. Sheedy FJ, Palsson-McDermott E, Hennessy EJ, Martin C, O'Leary JJ, Ruan Q, Johnson DS, Chen Y & O'Neill LA 2010 Negative regulation of TLR4 via targeting of the proinflammatory tumor suppressor PDCD4 by the microRNA miR-21. Nature Immunology 11 141-147. (doi:10.1038/ni.1828)
56. da Silveira JC, Veeramachaneni DNR, Winger QA, Carnevale EM & Bouma GJ 2012 Cell-secreted vesicles in equine ovarian follicular fluid contain miRNAs and proteins: a possible new form of cell communication within the ovarian follicle. Biology of Reproduction 86 71. (doi:10.1095/biolreprod.111.093252)
57. Sirotkin AV, Ovcharenko D, Grossmann R, Laukova M & Mlyncek M 2009 Identification of microRNAs controlling human ovarian cell steroidogenesis via a genome-scale screen. Journal of Cellular Physiology 219 415-420. (doi:10.1002/jcp.21689)
58. Sirotkin AV, Laukova M, Ovcharenko D, Brenaut P & Mlyncek M 2010 Identification of microRNAs controlling human ovarian cell proliferation and apoptosis. Journal of Cellular Physiology 223 49-56.
59. Stocco C, Telleria C & Gibori G 2007 The molecular control of corpus luteum formation, function, and regression. Endocrine Reviews 28 117-149. (doi:10.1210/er.2006-0022)
60. Suarez Y & Sessa WC 2009 MicroRNAs as novel regulators of angiogenesis. Circulation Research 104 442-454. (doi:10.1161/CIRCRESAHA.108. 191270)
61. Suh N, Baehner L, Moltzahn F, Melton C, Shenoy A, Chen J & Blelloch R 2010 MicroRNA function is globally suppressed in mouse oocytes and early embryos. Current Biology 20 271-277. (doi:10.1016/j.cub. 2009.12.044)
62. Tesfaye D, Worku D, Rings F, Phatsara C, Tholen E, Schellander K & Hoelker M 2009 Identification and expression profiling of microRNAs during bovine oocyte maturation using heterologous approach. Molecular Reproduction and Development 76 665-677. (doi:10.1002/mrd.21005)
63. Thomas M, Lieberman J & Lal A 2010 Desperately seeking microRNA targets. Nature Structural and Molecular Biology 17 1169-1174. (doi:10.1038/ nsmb.1921)
64. Thum T, Gross C, Fiedler J, Fischer T, Kissler S, Bussen M, Galuppo P, Just S, Rottbauer W, Frantz S et al. 2008 MicroRNA-21 contributes to myocardial disease by stimulating MAP kinase signalling in fibroblasts. Nature 456 980-984. (doi:10.1038/nature07511)
65. Tripurani SK, Xiao C, Salem M & Yao J 2010 Cloning and analysis of fetal ovary microRNAs in cattle. Animal Reproduction Science 120 16-22. (doi:10.1016/j.anireprosci.2010.03.001)
66. Wang K, Zhang S, Marzolf B, Troisch P, Brightman A, Hu Z, Hood LE & Galas DJ 2009 Circulating microRNAs, potential biomarkers for drug-induced liver injury. PNAS 106 4402-4407. (doi:10.1073/pnas. 0813371106)
67. Wang W, Chen X, Li X, Wang L, Zhang H, He Y, Wang J, Zhao Y, Zhang B & Xu Y 2011 Interference RNA-based silencing of endogenous SMAD4 in porcine granulosa cells resulted in decreased FSH-mediated granulosa cells proliferation and steroidogenesis. Reproduction 141 643-651. (doi:10.1530/ REP-10-0098)
68. Witwer KW, Sisk JM, Gama L & Clements JE 2010 MicroRNA regulation of IFN-b protein expression: rapid and sensitive modulation of the innate immune response. Journal of Immunology 184 2369-2376. (doi:10.4049/ jimmunol.0902712)
69. Wu YL & Wiltbank MC 2002 Transcriptional regulation of the cyclooxygenase-2 gene changes from protein kinase (PK) A-to PKCdependence after luteinization of granulosa cells. Biology of Reproduction 66 1505-1514. (doi:10.1095/biolreprod66.5.1505)
70. Wu YH, Hu TF, Chen YC, Tsai YN, Tsai YH, Cheng CC &WangHW2011 The manipulation of miRNA-gene regulatory networks by KSHV induces endothelial cell motility. Blood 118 2896-2905. (doi:10.1182/blood-2011-01-330589)
71. Xu S, Linher-Melville K, Yang BB, Wu D & Li J 2011 Micro-RNA378 (miR-378) regulates ovarian estradiol production by targeting aromatase. Endocrinology 152 3941-3951. (doi:10.1210/en.2011-1147)
72. Yan G, Zhang L, Fang T, Zhang Q, Wu S, Jiang Y, Sun H & Hu Y 2012 MicroRNA-145 suppresses mouse granulosa cell proliferation by targeting activin receptor IB. FEBS Letters 586 3263-3270. (doi:10.1016/j.febslet. 2012.06.048)
73. Yang X, Zhou Y, Peng S, Wu L, Lin H-Y, Wang S & Wang H 2012 Differentially expressed plasma microRNAs in premature ovarian failure patients and the potential regulatory function of mir-23a in granulosa cell apoptosis. Reproduction 144 235-244. (doi:10.1530/ REP-11-0371)
74. YaoN, LuCL, Zhao JJ,XiaHF, SunDG, Shi XQ,WangC, LiD, CuiY&MaX 2009 A network of miRNAs expressed in the ovary are regulated by FSH. Frontiers in Bioscience 14 3239-3245. (doi:10.2741/3447)
75. Yao G, Yin M, Lian J, Tian H, Liu L, Li X & Sun F 2010a MicroRNA-224 is involved in transforming growth factor-b-mediated mouse granulosa cell proliferation and granulosa cell function by targeting Smad4. Molecular Endocrinology 24 540-551. (doi:10.1210/me.2009-0432)
76. Yao N, Yang BQ, Liu Y, Tan XY, Lu CL, Yuan XH & Ma X 2010b Folliclestimulating hormone regulation of microRNA expression on progesterone production in cultured rat granulosa cells. Endocrine 38 158-166. (doi:10.1007/s12020-010-9345-1)
77. Yin M,Lu M, Yao G, Tian H, Lian J, Liu L, Liang M, Wang Y & Sun F 2012 Transactivation of microRNA-383 by steroidogenic factor-1 promotes estradiol release from mouse ovarian granulosa cells by targeting RBMS1. Molecular Endocrinology 26 1129-1143. (doi:10.1210/ me.2011-1341)