MicroRNA 376a regulates follicle assembly by targeting Pcna in fetal and neonatal mouse ovaries

Reproduction

Volumn 148, Issue 1, 2014, Pages 43-54

  Zhang, Huan ^a   Jiang, Xiaohua ^a   Zhang, Yuanwei ^a   Xu, Bo ^a   Hua, Juan ^a   Ma, Tieliang ^a   Zheng, Wei ^a   Sun, Rui ^a   Shen, Wei ^b   Cooke, Howard J ^a,c   Hao, Qiaomei ^a   Qiao, Jie ^d   Shi, Qinghua ^a  

^a UNIVERSITY OF SCIENCE AND TECHNOLOGY OF CHINA   (China)

^b QINGDAO AGRICULTURAL UNIVERSITY   (China)

^c UNIVERSITY OF EDINBURGH   (United Kingdom)

^d PEKING UNIVERSITY THIRD HOSPITAL   (China)

Author keywords

[No Author keywords available]

Indexed keywords

CYCLINE; MESSENGER RNA; MICRORNA; MICRORNA 376A; UNCLASSIFIED DRUG; 3' UNTRANSLATED REGION; MIRN376 MICRORNA, MOUSE;

3' UNTRANSLATED REGION; ANIMAL EXPERIMENT; APOPTOSIS; ARTICLE; CELL PROLIFERATION; COITUS; CONTROLLED STUDY; FEMALE; GENE OVEREXPRESSION; GENETIC TRANSFECTION; HEK293 CELL LINE; HUMAN; HUMAN CELL; MOUSE; NONHUMAN; OOCYTE; OOCYTE DEVELOPMENT; OVARY FOLLICLE; OVARY FOLLICLE DEVELOPMENT; PRIORITY JOURNAL; ANIMAL; BINDING SITE; EMBRYOLOGY; GENE EXPRESSION REGULATION; GENETICS; GESTATIONAL AGE; INSTITUTE FOR CANCER RESEARCH MOUSE; METABOLISM; NEWBORN; OVARY; RNA INTERFERENCE; SIGNAL TRANSDUCTION; TISSUE CULTURE TECHNIQUE;

3' UNTRANSLATED REGIONS; ANIMALS; ANIMALS, NEWBORN; APOPTOSIS; BINDING SITES; FEMALE; GENE EXPRESSION REGULATION, NEOPLASTIC; GESTATIONAL AGE; HEK293 CELLS; HUMANS; MICE, INBRED ICR; MICRORNAS; OVARIAN FOLLICLE; OVARY; PROLIFERATING CELL NUCLEAR ANTIGEN; RNA INTERFERENCE; SIGNAL TRANSDUCTION; TISSUE CULTURE TECHNIQUES; TRANSFECTION;

EID: 84903641859     PISSN: 14701626     EISSN: 17417899     Source Type: Journal    
DOI: 10.1530/REP-13-0508     Document Type: Article

References (77)

1. AhnHW, Morin RD, ZhaoH,Harris RA, Coarfa C, Chen ZJ, Milosavljevic A, Marra MA & Rajkovic A 2010 MicroRNA transcriptome in the newborn mouse ovaries determined by massive parallel sequencing. Molecular Human Repoduction 16 463-471. (doi:10.1093/molehr/gaq017)
2. Baker TG 1963 A quantitative and cytological study of germ cells in human ovaries. Proceedings of the Royal Society of London. Series B, Biological Sciences 158 417-433. (doi:10.1098/rspb.1963.0055)
3. Baley J & Li J 2012 MicroRNAs and ovarian function. Journal of Ovarian Research 5 8. (doi:10.1186/1757-2215-5-8)
4. Balla M, Angelopoulou R, Lavranos G & Kittas C 2008 Follicular cells versus oocytes: cell population dynamics in the developing ovary. Tissue & Cell 40 373-381. (doi:10.1016/j.tice.2008.03.006)
5. Bartel DP 2009 MicroRNAs: target recognition and regulatory functions. Cell 136 215-233. (doi:10.1016/j.cell.2009.01.002)
6. Bergeron L, Perez GI, Macdonald G, Shi L, Sun Y, Jurisicova A, Varmuza S, Latham KE, Flaws JA, Salter JC et al. 1998 Defects in regulation of apoptosis in caspase-2-deficient mice. Genes and Development 12 1304-1314. (doi:10.1101/gad.12.9.1304) (Pubitemid 28213406)
7. Betel D, Wilson M, Gabow A, Marks DS & Sander C 2008 The microRNA.org resource: targets and expression. Nucleic Acids Research 36 D149-D153. (doi:10.1093/nar/gkm995) (Pubitemid 351149712)
8. Borum K 1961 Oogenesis in the mouse. A study of the meiotic prophase. Experimental Cell Research 24 495-507. (doi:10.1016/0014-4827(61) 90449-9)
9. Broekmans FJ, Knauff EA, te Velde ER, Macklon NS & Fauser BC 2007 Female reproductive ageing: current knowledge and future trends. Trends in Endocrinology and Metabolism 18 58-65. (doi:10.1016/j.tem.2007. 01.004) (Pubitemid 46275460)
10. 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)
11. Chang CD, Ottavio L, Travali S, Lipson KE & Baserga R 1990 Transcriptional and posttranscriptional regulation of the proliferating cell nuclear antigen gene. Molecular and Cellular Biology 10 3289-3296.
12. Chen Y, Jefferson WN, Newbold RR, Padilla-Banks E & Pepling ME 2007 Estradiol, progesterone, and genistein inhibit oocyte nest breakdown and primordial follicle assembly in the neonatal mouse ovary in vitro and in vivo. Endocrinology 148 3580-3590. (doi:10.1210/en.2007-0088) (Pubitemid 47105867)
13. Choi Y, Qin Y, Berger MF, Ballow DJ, Bulyk ML & Rajkovic A 2007 Microarray analyses of newborn mouse ovaries lacking Nobox. Biology of Reproduction 77 312-319. (doi:10.1095/biolreprod.107.060459) (Pubitemid 47173614)
14. Choi Y, Ballow DJ, Xin Y & Rajkovic A 2008 Lim homeobox gene, lhx8, is essential for mouse oocyte differentiation and survival. Biology of Reproduction 79 442-449. (doi:10.1095/biolreprod.108.069393)
15. Corney DC, Flesken-Nikitin A, Godwin AK, Wang W & Nikitin AY 2007 MicroRNA-34b and microRNA-34c are targets of p53 and cooperate in control of cell proliferation and adhesion-independent growth. Cancer Research 67 8433-8438. (doi:10.1158/0008-5472.CAN-07-1585) (Pubitemid 47437414)
16. Coucouvanis EC, Sherwood SW, Carswell-Crumpton C, Spack EG & Jones PP 1993 Evidence that the mechanism of prenatal germ cell death in the mouse is apoptosis. Experimental Cell Research 209 238-247. (doi:10.1006/excr.1993.1307) (Pubitemid 24005308)
17. De Felici M, Lobascio AM & Klinger FG 2008 Cell death in fetal oocytes: many players for multiple pathways. Autophagy 4 240-242. (Pubitemid 351231190)
18. De Pol A, Vaccina F, Forabosco A, Cavazzuti E & Marzona L 1997 Apoptosis of germ cells during human prenatal oogenesis. Human Reproduction 12 2235-2241. (doi:10.1093/humrep/12.10.2235) (Pubitemid 27494035)
19. Essers J, Theil AF, Baldeyron C, van Cappellen WA, Houtsmuller AB, Kanaar R & Vermeulen W 2005 Nuclear dynamics of PCNA in DNA replication and repair. Molecular and Cellular Biology 25 9350-9359. (doi:10.1128/MCB.25.21. 9350-9359.2005) (Pubitemid 41507836)
20. Faddy MJ & Gosden RG 1996 A model conforming the decline in follicle numbers to the age of menopause in women. Human Reproduction 11 1484-1486. (doi:10.1093/oxfordjournals.humrep.a019422) (Pubitemid 26335098)
21. Faddy MJ, Gosden RG, Gougeon A, Richardson SJ & Nelson JF 1992 Accelerated disappearance of ovarian follicles in mid-life: implications for forecasting menopause. Human Reproduction 7 1342-1346. (Pubitemid 23042150)
22. Flaws JA, Hirshfield AN, Hewitt JA, Babus JK & Furth PA 2001 Effect of bcl-2 on the primordial follicle endowment in the mouse ovary. Biology of Reproduction 64 1153-1159. (doi:10.1095/biolreprod64. 4.1153) (Pubitemid 32239186)
23. Fujiwara Y, Komiya T, Kawabata H, Sato M, Fujimoto H, Furusawa M & Noce T 1994 Isolation of a DEAD-family protein gene that encodes a murine homolog of Drosophila vasa and its specific expression in germ cell lineage. PNAS 91 12258-12262. (doi:10.1073/pnas.91.25.12258) (Pubitemid 24368644)
24. Gammell P 2007 MicroRNAs: recently discovered key regulators of proliferation and apoptosis in animal cells: identification of miRNAs regulating growth and survival. Cytotechnology 53 55-63. (doi:10.1007/ s10616-007-9049-4) (Pubitemid 46944869)
25. Grentzmann G, Ingram JA, Kelly PJ, Gesteland RF & Atkins JF 1998 A dual-luciferase reporter system for studying recoding signals. RNA 4 479-486. (doi:10.1017/S1355838298971576) (Pubitemid 28359767)
26. Han L, Zhang A, Zhou X, Xu P, Wang GX, Pu PY & Kang CS 2010 Downregulation of Dicer enhances tumor cell proliferation and invasion. International Journal of Oncology 37 299-305. (doi:10.3892/Ijo-00000678)
27. Higuchi R, Krummel B & Saiki RK 1988 A general method of in vitro preparation and specific mutagenesis of DNA fragments: study of protein and DNA interactions. Nucleic Acids Research 16 7351-7367. (doi:10.1093/nar/16.15.7351)
28. 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 micro-RNAs in testicular and ovarian tissues in Holstein cattle. International Journal of Biological Sciences 7 1016-1026. (doi:10.7150/ijbs.7.1016)
29. 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)
30. Hutt KJ, McLaughlin EA & Holland MK 2006 Primordial follicle activation and follicular development in the juvenile rabbit ovary. Cell and Tissue Research 326 809-822. (doi:10.1007/s00441-006-0223-3) (Pubitemid 44786379)
31. Johnson J, Canning J, Kaneko T, Pru JK & Tilly JL 2004 Germline stem cells and follicular renewal in the postnatal mammalian ovary. Nature 428 145-150. (doi:10.1038/nature02316) (Pubitemid 38374304)
32. Kerr JB, Duckett R, Myers M, Britt KL, Mladenovska T & Findlay JK 2006 Quantification of healthy follicles in the neonatal and adult mouse ovary: evidence for maintenance of primordial follicle supply. Reproduction 132 95-109. (doi:10.1530/rep.1.01128) (Pubitemid 44123387)
33. Kim SY, Cordeiro MH, Serna VA, Ebbert K, Butler LM, Sinha S, Mills AA, Woodruff TK & Kurita T 2013 Rescue of platinum-damaged oocytes from programmed cell death through inactivation of the p53 family signaling network. Cell Death and Differentiation 20 987-997. (doi:10.1038/cdd.2013.31)
34. Korfsmeier KH 2002 PCNA in the ovary of zebrafish (Brachydanio rerio, Ham.-Buch.). Acta Histochemica 104 73-76. (doi:10.1078/0065-1281-00632)
35. Krol J, Loedige I & Filipowicz W 2010 The widespread regulation of microRNA biogenesis, function and decay. Nature Reviews. Genetics 11 597-610. (doi:10.1038/Nrg2843)
36. 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)
37. Liang C, Zhu H, Xu Y, Huang L, Ma C, Deng W, Liu Y & Qin C 2011 MicroRNA-153 negatively regulates the expression of amyloid precursor protein and amyloid precursor-like protein 2. Brain Research 1455 103-113. (doi:10.1016/j.brainres.2011.10.051)
38. Lobascio AM, Klinger FG, Scaldaferri ML, Farini D & De Felici M 2007 Analysis of programmed cell death in mouse fetal oocytes. Reproduction 134 241-252. (doi:10.1530/REP-07-0141) (Pubitemid 47278797)
39. Maheshwari A & Fowler PA 2008 Primordial follicular assembly in humans - revisited. Zygote 16 285-296. (doi:10.1017/S0967199408004802)
40. Matikainen T, Perez GI, Zheng TS, Kluzak TR, Rueda BR, Flavell RA & Tilly JL 2001 Caspase-3 gene knockout defines cell lineage specificity for programmed cell death signaling in the ovary. Endocrinology 142 2468-2480. (doi:10.1210/en.142.6.2468) (Pubitemid 32473103)
41. Meredith S, Dudenhoeffer G & Jackson K 2000 Classification of small type B/C follicles as primordial follicles in mature rats. Journal of Reproduction and Fertility 119 43-48. (doi:10.1530/reprod/119.1.43) (Pubitemid 30312726)
42. Morita Y, Maravei DV, Bergeron L, Wang S, Perez GI, Tsutsumi O, Taketani Y, Asano M, Horai R, Korsmeyer SJ et al. 2001 Caspase-2 deficiency prevents programmed germ cell death resulting from cytokine insufficiency but not meiotic defects caused by loss of ataxia telangiectasia-mutated (Atm) gene function. Cell Death and Differentiation 8 614-620. (doi:10.1038/sj.cdd.4400845) (Pubitemid 32586598)
43. Murchison EP, Stein P, Xuan Z, Pan H, Zhang MQ, Schultz RM & Hannon GJ 2007 Critical roles for Dicer in the female germline. Genes and Development 21 682-693. (doi:10.1101/gad.1521307) (Pubitemid 46440290)
44. Muskhelishvili L, Wingard SK & Latendresse JR 2005 Proliferating cell nuclear antigen - a marker for ovarian follicle counts. Toxicologic Pathology 33 365-368. (doi:10.1080/01926230590930164) (Pubitemid 40617140)
45. Nilsson E, Rogers N & Skinner MK 2007 Actions of anti-Mullerian hormone on the ovarian transcriptome to inhibit primordial to primary follicle transition. Reproduction 134 209-221. (doi:10.1530/REP-07-0119) (Pubitemid 47278794)
46. Oktay K, Schenken RS & Nelson JF 1995 Proliferating cell nuclear antigen marks the initiation of follicular growth in the rat. Biology of Reproduction 53 295-301. (doi:10.1095/biolreprod53.2.295)
47. Omer AD, Janas MM & Novina CD 2009 The chicken or the egg: microRNA-mediated regulation of mRNA translation or mRNA stability. Molecular Cell 35 739-740. (doi:10.1016/j.molcel.2009.09.003)
48. 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) (Pubitemid 351632396)
49. Paddison PJ, Silva JM, Conklin DS, Schlabach M, Li M, Aruleba S, Balija V, O'Shaughnessy A, Gnoj L, Scobie K et al. 2004 A resource for large-scale RNA-interference-based screens in mammals. Nature 428 427-431. (doi:10.1038/nature02370) (Pubitemid 38419688)
50. Pepling ME 2006 From primordial germ cell to primordial follicle: mammalian female germ cell development. Genesis 44 622-632. (doi:10.1002/dvg. 20258) (Pubitemid 46047873)
51. Pepling ME & Spradling AC 2001 Mouse ovarian germ cell cysts undergo programmed breakdown to form primordial follicles. Developmental Biology 234 339-351. (doi:10.1006/dbio.2001.0269) (Pubitemid 32552663)
52. Pesce M & De Felici M 1994 Apoptosis in mouse primordial germ cells: a study by transmission and scanning electron microscope. Anatomy and Embryology 189 435-440. (doi:10.1007/BF00185438) (Pubitemid 24163632)
53. Picut CA, Swanson CL, Scully KL, Roseman VC, Parker RF & Remick AK 2008 Ovarian follicle counts using proliferating cell nuclear antigen (PCNA) and semi-automated image analysis in rats. Toxicologic Pathology 36 674-679. (doi:10.1177/0192623308317428)
54. Raschzok N, Werner W, Sallmon H, Billecke N, Dame C, Neuhaus P & Sauer IM 2011 Temporal expression profiles indicate a primary function for microRNA during the peak of DNA replication after rat partial hepatectomy. American Journal of Physiology. Regulatory, Integrative and Comparative Physiology 300 R1363-R1372. (doi:10.1152/ajpregu.00632.2010)
55. Ratts VS, Flaws JA, Kolp R, Sorenson CM & Tilly JL 1995 Ablation of bcl-2 gene expression decreases the numbers of oocytes and primordial follicles established in the post-natal female mouse gonad. Endocrinology 136 3665-3668. (doi:10.1210/endo.136.8.7628407)
56. Reddy P, Liu L, Adhikari D, Jagarlamudi K, Rajareddy S, Shen Y, Du C, Tang W, Hamalainen T, Peng SL et al. 2008 Oocyte-specific deletion of Pten causes premature activation of the primordial follicle pool. Science 319 611-613. (doi:10.1126/science.1152257) (Pubitemid 351197061)
57. Ricci EP, Limousin T, Soto-Rifo R, Allison R, Poyry T, Decimo D, Jackson RJ & Ohlmann T 2011 Activation of a microRNA response in trans reveals a new role for poly(A) in translational repression. Nucleic Acids Research 39 5215-5231. (doi:10.1093/nar/gkr086)
58. 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) (Pubitemid 350127576)
59. Robker RL & Richards JS 1998 Hormone-induced proliferation and differentiation of granulosa cells: a coordinated balance of the cell cycle regulators cyclin D2 and p27Kip1. Molecular Endocrinology 12 924-940. (doi:10.1210/mend.12.7.0138) (Pubitemid 30660661)
60. Rodrigues P, Limback D, McGinnis LK, Plancha CE & Albertini DF 2009 Multiple mechanisms of germ cell loss in the perinatal mouse ovary. Reproduction 137 709-720. (doi:10.1530/REP-08-0203)
61. Rucker EB III, Dierisseau P, Wagner KU, Garrett L, Wynshaw-Boris A, Flaws JA & Hennighausen L 2000 Bcl-x and Bax regulatemouse primordial germ cell survival and apoptosis during embryogenesis. Molecular Endocrinology 14 1038-1052. (doi:10.1210/mend.14.7.0465) (Pubitemid 32250520)
62. Shen W, Li L, Bai Z, Pan Q,Ding M&Deng H 2007 In vitro development of mouse fetal germ cells into mature oocytes. Reproduction 134 223-231. (doi:10.1530/REP-06-0378) (Pubitemid 47278795)
63. 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. (doi:10.1002/jcp.21999)
64. Sullivan SD & Castrillon DH 2011 Insights into primary ovarian insufficiency through genetically engineered mouse models. Seminars in Reproductive Medicine 29 283-298. (doi:10.1055/s-0031-1280914)
65. Torley KJ, da Silveira JC, Smith P, Anthony RV, Veeramachaneni DN, Winger QA & Bouma GJ 2011 Expression of miRNAs in ovine fetal gonads: potential role in gonadal differentiation. Reproductive Biology and Endocrinology 9 2. (doi:10.1186/1477-7827-9-2)
66. 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)
67. Wang C & Roy SK 2006 Expression of growth differentiation factor 9 in the oocytes is essential for the development of primordial follicles in the hamster ovary. Endocrinology 147 1725-1734. (doi:10.1210/en.2005-1208)
68. Wang Y & Lee CG 2009 MicroRNA and cancer - focus on apoptosis. Journal of Cellular and Molecular Medicine 13 12-23. (doi:10.1111/ j.1582-4934.2008.00510.x)
69. Wen J, Zhang H, Li G, Mao G, Chen X, Wang J, Guo M, Mu X, Ouyang H, Zhang M et al. 2009 PAR6, a potential marker for the germ cells selected to form primordial follicles in mouse ovary. PLoS ONE 4 e7372. (doi:10. 1371/journal.pone.0007372)
70. Wu L, Fan J & Belasco JG 2006 MicroRNAs direct rapid deadenylation of mRNA. PNAS 103 4034-4039. (doi:10.1073/pnas.0510928103)
71. Wu E, Thivierge C, FlamandM, Mathonnet G, Vashisht AA,Wohlschlegel J, Fabian MR, Sonenberg N & Duchaine TF 2010 Pervasive and cooperative deadenylation of 30UTRs by embryonic microRNA families. Molecular Cell 40 558-570. (doi:10.1016/j.molcel.2010.11.003)
72. Xu B, Hua J, Zhang Y, Jiang X, Zhang H, Ma T, Zheng W, Sun R, Shen W, Sha J et al. 2011a Proliferating cell nuclear antigen (PCNA) regulates primordial follicle assembly by promoting apoptosis of oocytes in fetal and neonatal mouse ovaries. PLoS ONE 6 e16046. (doi:10.1371/journal.pone.0016046)
73. Xu S, Linher-Melville K, Yang BB,Wu D & Li J 2011b Micro-RNA378 (miR- 378) regulates ovarian estradiol production by targeting aromatase. Endocrinology 152 3941-3951. (doi:10.1210/en.2011-1147)
74. Zenz T, Mohr J, Eldering E, Kater AP, Buhler A, Kienle D, Winkler D, Durig J, van Oers MH, Mertens D et al. 2009 miR-34a as part of the resistance network in chronic lymphocytic leukemia. Blood 113 3801-3808. (doi:10.1182/blood-2008-08-172254)
75. Zhang Z, Shen B,Wang Y, Chen Y,Wang G, Lin P & Zou Z 2010 Molecular cloning of proliferating cell nuclear antigen and its differential expression analysis in the developing ovary and testis of penaeid shrimp Marsupenaeus japonicus. DNA and Cell Biology 29 163-170. (doi:10.1089/dna.2009.0958)
76. Zhang Y, Yang Y, Zhang H, Jiang X, Xu B, Xue Y, Cao Y, ZhaiQ, Zhai Y, XuM et al. 2011 Prediction of novel pre-microRNAs with high accuracy through boosting and SVM. Bioinformatics 27 1436-1437. (doi:10.1093/bioinformatics/ btr148)
77. Zhang J, Ji X, Zhou D, Li Y, Lin J, Liu J, Luo H & Cui S 2013 miR-143 is critical for the formation of primordial follicles in mice. Frontiers in Bioscience 18 588-597. (doi:10.2741/4122)