Expression patterns and regulatory functions of microRNAs during the initiation of primordial follicle development in the neonatal mouse ovary

Biology of Reproduction

Volumn 89, Issue 5, 2013, Pages

  Yang, Shuhong ^a   Wang, Shuo ^a   Luo, Aiyue ^a   Ding, Ting ^a   Lai, Zhiwen ^a   Shen, Wei ^a   Ma, Xiangyi ^a   Cao, Chen ^a   Shi, Liangyan ^a   Jiang, Jingjing ^a   Rong, Fangfang ^a   Ma, Lanfang ^a   Tian, Yong ^a   Du, Xiaofang ^a   Lu, Yunping ^a   Li, Ya ^a   Wang, Shixuan ^a  

^a HUAZHONG UNIVERSITY OF SCIENCE AND TECHNOLOGY   (China)

Author keywords

miR 145; p Smad3; Primordial follicle initiation; TGF signaling pathway

Indexed keywords

ANTAGOMIR; MICRORNA; MICRORNA 145; TRANSFORMING GROWTH FACTOR BETA; TRANSFORMING GROWTH FACTOR BETA RECEPTOR 2;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONFOCAL MICROSCOPY; CONTROLLED STUDY; DOWN REGULATION; FEMALE; FEMALE FERTILITY; GENE CONTROL; GENE EXPRESSION; GENE ONTOLOGY; GENE TARGETING; IMMUNOHISTOCHEMISTRY; IN SITU HYBRIDIZATION; IN VITRO STUDY; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; OOCYTE MATURATION; OVARY; OVARY FOLLICLE; OVARY FOLLICLE DEVELOPMENT; PRIORITY JOURNAL; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RNA ANALYSIS; SIGNAL TRANSDUCTION; UPREGULATION;

MIR-145; P-SMAD3; PRIMORDIAL FOLLICLE INITIATION; TGF-Β SIGNALING PATHWAY;

ANIMALS; ANIMALS, NEWBORN; CELL DIFFERENTIATION; FEMALE; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENE REGULATORY NETWORKS; MICE; MICE, INBRED C57BL; MICROARRAY ANALYSIS; MICRORNAS; OVARIAN FOLLICLE; OVARY;

EID: 84901034798     PISSN: 00063363     EISSN: 15297268     Source Type: Journal    
DOI: 10.1095/biolreprod.113.107730     Document Type: Article

References (52)

1. Hansen KR, Knowlton NS, Thyer AC, Charleston JS, Soules MR, Klein NA. A new model of reproductive aging: the decline in ovarian nongrowing follicle number from birth to menopause. Hum Reprod 2008; 23: 699-708.
2. Broekmans FJ, Knauff EA, te Velde ER, Macklon NS, Fauser BC. Female reproductive ageing: current knowledge and future trends. Trends Endocrinol Metab 2007; 18:58-65.
3. Sutherland JM, Keightley RA, Nixon B, Roman SD, Robker RL, Russell DL, McLaughlin EA. Suppressor of cytokine signaling 4 (SOCS4): moderator of ovarian primordial follicle activation. J Cell Physiol 2012; 227:1188-1198.
4. Oktem O, Urman B. Understanding follicle growth in vivo. Hum Reprod 2010; 25:2944-2954.
5. Adhikari D, Liu K. Molecular mechanisms underlying the activation of mammalian primordial follicles. Endocr Rev 2009; 30:438-464.
6. Du T, Zamore PD. microPrimer: the biogenesis and function of microRNA. Development 2005; 132:4645-4652.
7. Toloubeydokhti T, Bukulmez O, Chegini N. Potential regulatory functions of microRNAs in the ovary. Semin Reprod Med 2008; 26:469-478.
8. Baley J, Li J. MicroRNAs and ovarian function. J Ovarian Res 2012; 5:8.
9. Luense LJ, Carletti MZ, Christenson LK. Role of Dicer in female fertility. Trends Endocrinol Metab 2009; 20:265-272.
10. Lei L, Jin S, Gonzalez G, Behringer RR, Woodruff TK. The regulatory role of Dicer in folliculogenesis in mice. Mol Cell Endocrinol 2010; 315: 63-73.
11. Hong X, Luense LJ, McGinnis LK, Nothnick WB, Christenson LK. Dicer1 is essential for female fertility and normal development of the female reproductive system. Endocrinology 2008; 149:6207-6212.
12. Nagaraja AK, Andreu-Vieyra C, Franco HL, Ma L, Chen R, Han DY, Zhu H, Agno JE, Gunaratne PH, DeMayo FJ, Matzuk MM. Deletion of Dicer in somatic cells of the female reproductive tract causes sterility. Mol Endocrinol 2008; 22:2336-2352.
13. Chen C, Ridzon DA, Broomer AJ, Zhou Z, Lee DH, Nguyen JT, Barbisin M, Xu NL, Mahuvakar VR, Andersen MR, Lao KQ, Livak KJ, et al. Realtime quantification of microRNAs by stem-loop RT-PCR. Nucleic Acids Res 2005; 33:e179.
14. Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods 2001; 25:402-408.
15. Yang S, Luo A, Hao X, Lai Z, Ding T, Ma X, Mayinuer M, Shen W, Wang X, Lu Y, Ma D, Wang S. Peroxiredoxin 2 inhibits granulosa cell apoptosis during follicle atresia through the NFKB pathway in mice. Biol Reprod 2011; 84:1182-1189.
16. Parrott JA, Skinner MK. Kit-ligand/stem cell factor induces primordial follicle development and initiates folliculogenesis. Endocrinology 1999; 140:4262-4271.
17. Wright GW, Simon RM. A random variance model for detection of differential gene expression in small microarray experiments. Bioinformatics 2003; 19:2448-2455.
18. Kim JY. Control of ovarian primordial follicle activation. Clin Exp Reprod Med 2012; 39:10-14.
19. Pangas SA. Regulation of the ovarian reserve by members of the transforming growth factor beta family. Mol Reprod Dev 2012; 79: 666-679.
20. Krutzfeldt J, Rajewsky N, Braich R, Rajeev KG, Tuschl T, Manoharan M, Stoffel M. Silencing of microRNAs in vivo with 'antagomirs.' Nature 2005; 438:685-689.
21. Otsuka M, Zheng M, Hayashi M, Lee JD, Yoshino O, Lin S, Han J. Impaired microRNA processing causes corpus luteum insufficiency and infertility in mice. J Clin Invest 2008; 118:1944-1954.
22. Sirotkin AV, Ovcharenko D, Grossmann R, Laukova M, Mlyncek M. Identification of microRNAs controlling human ovarian cell steroidogenesis via a genome-scale screen. J Cell Physiol 2009; 219:415-420.
23. Xu S, Linher-Melville K, Yang BB, Wu D, Li J. Micro-RNA378 (miR-378) regulates ovarian estradiol production by targeting aromatase. Endocrinology 2011; 152:3941-3951.
24. Ma T, Jiang H, Gao Y, Zhao Y, Dai L, Xiong Q, Xu Y, Zhao Z, Zhang J. 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. J Appl Genet 2011; 52:481-486.
25. Li-Ping Z, Da-Lei Z, Jian H, Liang-Quan X, Ai-Xia X, Xiao-Yu D, Dan-Feng T, Yue-Hui Z. Proto-oncogene c-erbB2 initiates rat primordial follicle growth via PKC and MAPK pathways. Reprod Biol Endocrinol 2010; 8:66.
26. Kezele PR, Ague JM, Nilsson E, Skinner MK. Alterations in the ovarian transcriptome during primordial follicle assembly and development. Biol Reprod 2005; 72:241-255.
27. Roberts AE, Arbogast LK, Friedman CI, Cohn DE, Kaumaya PT, Danforth DR. Neutralization of endogenous vascular endothelial growth factor depletes primordial follicles in the mouse ovary. Biol Reprod 2007; 76:218-223.
28. McFee RM, Artac RA, Clopton DT, Smith RA, Rozell TG, Cupp AS. Inhibition of vascular endothelial growth factor receptor signal transduction blocks follicle progression but does not necessarily disrupt vascular development in perinatal rat ovaries. Biol Reprod 2009; 81:966-977.
29. Adhikari D, Flohr G, Gorre N, Shen Y, Yang H, Lundin E, Lan Z, Gambello MJ, Liu K. Disruption of Tsc2 in oocytes leads to overactivation of the entire pool of primordial follicles. Mol Hum Reprod 2009; 15: 765-770.
30. Adhikari D, Liu K. mTOR signaling in the control of activation of primordial follicles. Cell Cycle 2010; 9:1673-1674.
31. Trombly DJ, Woodruff TK, Mayo KE. Roles for transforming growth factor beta superfamily proteins in early folliculogenesis. Semin Reprod Med 2009; 27:14-23.
32. Nilsson EE, Schindler R, Savenkova MI, Skinner MK. Inhibitory actions of anti-Mullerian hormone (AMH) on ovarian primordial follicle assembly. PLoS One 2011; 6:e20087.
33. Ding CC, Thong KJ, Krishna A, Telfer EE. Activin A inhibits activation of human primordial follicles in vitro. J Assist Reprod Genet 2010; 27: 141-147.
34. Nilsson EE, Skinner MK. Bone morphogenetic protein-4 acts as an ovarian follicle survival factor and promotes primordial follicle development. Biol Reprod 2003; 69:1265-1272.
35. Kaivo-oja N, Jeffery LA, Ritvos O, Mottershead DG. Smad signalling in the ovary. Reprod Biol Endocrinol 2006; 4:21.
36. Michael MZ, O'Connor SM, van Holst Pellekaan NG, Young GP, James RJ. Reduced accumulation of specific microRNAs in colorectal neoplasia. Mol Cancer Res 2003; 1:882-891.
37. Iorio MV, Ferracin M, Liu CG, Veronese A, Spizzo R, Sabbioni S, Magri E, Pedriali M, Fabbri M, Campiglio M, Menard S, Palazzo JP, et al. MicroRNA gene expression deregulation in human breast cancer. Cancer Res 2005; 65:7065-7070.
38. Iorio MV, Visone R, Di Leva G, Donati V, Petrocca F, Casalini P, Taccioli C, Volinia S, Liu CG, Alder H, Calin GA, Menard S, et al. MicroRNA signatures in human ovarian cancer. Cancer Res 2007; 67:8699-8707.
39. Liu X, Sempere LF, Galimberti F, Freemantle SJ, Black C, Dragnev KH, Ma Y, Fiering S, Memoli V, Li H, DiRenzo J, Korc M, et al. Uncovering growth-suppressive MicroRNAs in lung cancer. Clin Cancer Res 2009; 15:1177-1183.
40. Schaefer A, Jung M, Mollenkopf HJ, Wagner I, Stephan C, Jentzmik F, Miller K, Lein M, Kristiansen G, Jung K. Diagnostic and prognostic implications of microRNA profiling in prostate carcinoma. Int J Cancer 2010; 126:1166-1176.
41. Takagi T, Iio A, Nakagawa Y, Naoe T, Tanigawa N, Akao Y. Decreased expression of microRNA-143 and-145 in human gastric cancers. Oncology 2009; 77:12-21.
42. Chen HC, Chen GH, Chen YH, Liao WL, Liu CY, Chang KP, Chang YS, Chen SJ. MicroRNA deregulation and pathway alterations in nasopharyngeal carcinoma. Br J Cancer 2009; 100:1002-1011.
43. Ichimi T, Enokida H, Okuno Y, Kunimoto R, Chiyomaru T, Kawamoto K, Kawahara K, Toki K, Kawakami K, Nishiyama K, Tsujimoto G, Nakagawa M, et al. Identification of novel microRNA targets based on microRNA signatures in bladder cancer. Int J Cancer 2009; 125:345-352.
44. Xu Q, Liu LZ, Qian X, Chen Q, Jiang Y, Li D, Lai L, Jiang BH. MiR-145 directly targets p70S6K1 in cancer cells to inhibit tumor growth and angiogenesis. Nucleic Acids Res 2012; 40:761-774.
45. Lintern-Moore S, Moore GP. The initiation of follicle and oocyte growth in the mouse ovary. Biol Reprod 1979; 20:773-778.
46. Wandji SA, Srsen V, Voss AK, Eppig JJ, Fortune JE. Initiation in vitro of growth of bovine primordial follicles. Biol Reprod 1996; 55:942-948.
47. Rojas A, Padidam M, Cress D, Grady WM. TGF-beta receptor levels regulate the specificity of signaling pathway activation and biological effects of TGF-beta. Biochim Biophys Acta 2009; 1793:1165-1173.
48. Tomic D, Brodie SG, Deng C, Hickey RJ, Babus JK, Malkas LH, Flaws JA. Smad 3 may regulate follicular growth in the mouse ovary. Biol Reprod 2002; 66:917-923.
49. Reddy P, Liu L, Adhikari D, Jagarlamudi K, Rajareddy S, Shen Y, Du C, Tang W, Hamalainen T, Peng SL, Lan ZJ, Cooney AJ, et al. Oocytespecific deletion of Pten causes premature activation of the primordial follicle pool. Science 2008; 319:611-613.
50. Liu CG, Calin GA, Meloon B, Gamliel N, Sevignani C, Ferracin M, Dumitru CD, Shimizu M, Zupo S, Dono M, Alder H, Bullrich F, et al. An oligonucleotide microchip for genome-wide microRNA profiling in human and mouse tissues. Proc Natl Acad Sci U S A 2004; 101: 9740-9744.
51. Dennis G Jr, Sherman BT, Hosack DA, Yang J, Gao W, Lane HC, Lempicki RA. DAVID: database for annotation, visualization, and integrated discovery. Genome Biol 2003; 4:P3.
52. Yao G, Yin M, Lian J, Tian H, Liu L, Li X, Sun F. MicroRNA-224 is involved in transforming growth factor-beta-mediated mouse granulosa cell proliferation and granulosa cell function by targeting Smad4. Mol Endocrinol 2010; 24:540-551.