Semin Reprod Med 2008; 26(6): 461-468
DOI: 10.1055/s-0028-1096126
© Thieme Medical Publishers

MicroRNAs and Mammalian Ovarian Development

Han Zhao1 , 2 , Aleksandar Rajkovic1
  • 1Department of Obstetrics and Gynecology, Baylor College of Medicine, Houston, Texas
  • 2Center for Reproductive Medicine, Shandong Provincial Hospital, Shandong Uni versity, Jinan, Shandong, China
Further Information

Publication History

Publication Date:
24 October 2008 (online)

ABSTRACT

Mammalian ovarian development involves unique interactions between the germ-line and somatic genomes. Several regulators affect gene expression, including a class of small RNAs called microRNAs (miRNAs). miRNAs are small, noncoding, regulatory RNAs that are 19 to 25 nucleotides long. miRNAs regulate gene expression in part via translational control of messenger RNAs (mRNAs). miRNAs are expressed during different stages of mammalian ovarian development and are likely to play important roles during gonadal development and folliculogenesis. The role of individual miRNAs in mammalian ovarian development is currently unknown and will remain an important focus for future investigations.

REFERENCES

  • 1 de Rooij D G, de Boer P. Specific arrests of spermatogenesis in genetically modified and mutant mice.  Cytogenet Genome Res. 2003;  103 267-276
  • 2 Pangas S A, Rajkovic A. Transcriptional regulation of early oogenesis: in search of masters.  Hum Reprod Update. 2006;  12 65-76
  • 3 Ford C E, Evans E P, Gardner R L. Marker chromosome analysis of two mouse chimaeras.  J Embryol Exp Morphol. 1975;  33 447-457
  • 4 Wilhelm D, Palmer S, Koopman P. Sex determination and gonadal development in mammals.  Physiol Rev. 2007;  87 1-28
  • 5 Wylie C. Germ cells.  Cell. 1999;  96 165-174
  • 6 Pepling M E, Spradling A C. Mouse ovarian germ cell cysts undergo programmed breakdown to form primordial follicles.  Dev Biol. 2001;  234 339-351
  • 7 Choi Y, Rajkovic A. Genetics of early mammalian folliculogenesis.  Cell Mol Life Sci. 2006;  63 579-590
  • 8 Parrott J A, Skinner M K. Kit-ligand/stem cell factor induces primordial follicle development and initiates folliculogenesis.  Endocrinology. 1999;  140 4262-4271
  • 9 Dong J, Albertini D F, Nishimori K, Kumar T R, Lu N, Matzuk M M. Growth differentiation factor-9 is required during early ovarian folliculogenesis.  , [see comments] Nature. 1996;  383 531-535
  • 10 Hanrahan J P, Gregan S M, Mulsant P et al.. Mutations in the genes for oocyte-derived growth factors GDF9 and BMP15 are associated with both increased ovulation rate and sterility in Cambridge and Belclare sheep (Ovis aries).  Biol Reprod. 2004;  70 900-909
  • 11 Matzuk M M, Lamb D J. Genetic dissection of mammalian fertility pathways.  Nat Cell Biol. 2002;  4(Suppl) s41-s49
  • 12 Mattick J S. The functional genomics of noncoding RNA.  Science. 2005;  309 1527-1528
  • 13 Okazaki Y, Furuno M, Kasukawa T et al.. Analysis of the mouse transcriptome based on functional annotation of 60,770 full-length cDNAs.  Nature. 2002;  420 563-573
  • 14 Reik W, Walter J. Genomic imprinting: parental influence on the genome.  Nat Rev Genet. 2001;  2 21-32
  • 15 Mattick J S, Gagen M J. The evolution of controlled multitasked gene networks: the role of introns and other noncoding RNAs in the development of complex organisms.  Mol Biol Evol. 2001;  18 1611-1630
  • 16 Lee R C, Feinbaum R L, Ambros V. The C. elegans heterochronic gene lin-4 encodes small RNAs with antisense complementarity to lin-14.  Cell. 1993;  75 843-854
  • 17 Tarn W Y, Steitz J A. Pre-mRNA splicing: the discovery of a new spliceosome doubles the challenge.  Trends Biochem Sci. 1997;  22 132-137
  • 18 Krause M, Hirsh D. A trans-spliced leader sequence on actin mRNA in C. elegans.  Cell. 1987;  49 753-761
  • 19 Murphy W J, Watkins K P, Agabian N. Identification of a novel Y branch structure as an intermediate in trypanosome mRNA processing: evidence for trans splicing.  Cell. 1986;  47 517-525
  • 20 Nilsen T W. Trans-splicing in protozoa and helminths.  Infect Agents Dis. 1992;  1 212-218
  • 21 Rajkovic A, Davis R E, Simonsen J N, Rottman F M. A spliced leader is present on a subset of mRNAs from the human parasite Schistosoma mansoni.  Proc Natl Acad Sci U S A. 1990;  87 8879-8883
  • 22 Sutton R E, Boothroyd J C. Evidence for trans splicing in trypanosomes.  Cell. 1986;  47 527-535
  • 23 Fire A, Xu S, Montgomery M K, Kostas S A, Driver S E, Mello C C. Potent and specific genetic interference by double-stranded RNA in Caenorhabditis elegans.  Nature. 1998;  391 806-811
  • 24 Elbashir S M, Harborth J, Lendeckel W, Yalcin A, Weber K, Tuschl T. Duplexes of 21-nucleotide RNAs mediate RNA interference in cultured mammalian cells.  Nature. 2001;  411 494-498
  • 25 Hannon G J, Rossi J J. Unlocking the potential of the human genome with RNA interference.  Nature. 2004;  431 371-378
  • 26 Stein P, Svoboda P, Schultz R M. Transgenic RNAi in mouse oocytes: a simple and fast approach to study gene function.  Dev Biol. 2003;  256 187-193
  • 27 Park C E, Lee D, Kim K H, Lee K A. Establishment of ovarian reconstruction system in culture for functional genomic analysis.  J Biosci Bioeng. 2006;  102 396-401
  • 28 McCaffrey A P, Meuse L, Pham T T, Conklin D S, Hannon G J, Kay M A. RNA interference in adult mice.  Nature. 2002;  418 38-39
  • 29 Lewis D L, Hagstrom J E, Loomis A G, Wolff J A, Herweijer H. Efficient delivery of siRNA for inhibition of gene expression in postnatal mice.  Nat Genet. 2002;  32 107-108
  • 30 Song E, Lee S K, Wang J et al.. RNA interference targeting Fas protects mice from fulminant hepatitis.  Nat Med. 2003;  9 347-351
  • 31 Sen C K, Roy S. miRNA: licensed to kill the messenger.  DNA Cell Biol. 2007;  26 193-194
  • 32 Marsden P A. RNA interference as potential therapy–not so fast.  N Engl J Med. 2006;  355 953-954
  • 33 Reinhart B J, Slack F J, Basson M et al.. The 21-nucleotide let-7 RNA regulates developmental timing in Caenorhabditis elegans.  Nature. 2000;  403 901-906
  • 34 Griffiths-Jones S. The microRNA Registry.  Nucleic Acids Res. 2004;  32(Database issue) D109-D111
  • 35 Hafner M, Landgraf P, Ludwig J et al.. Identification of microRNAs and other small regulatory RNAs using cDNA library sequencing.  Methods. 2008;  44 3-12
  • 36 Filipowicz W, Bhattacharyya S N, Sonenberg N. Mechanisms of post-transcriptional regulation by microRNAs: are the answers in sight?.  Nat Rev Genet. 2008;  9 102-114
  • 37 Du T, Zamore P D. microPrimer: the biogenesis and function of microRNA.  Development. 2005;  132 4645-4652
  • 38 Rana T M. Illuminating the silence: understanding the structure and function of small RNAs.  Nat Rev Mol Cell Biol. 2007;  8 23-36
  • 39 Peters L, Meister G. Argonaute proteins: mediators of RNA silencing.  Mol Cell. 2007;  26 611-623
  • 40 Jin P, Zarnescu D C, Ceman S et al.. Biochemical and genetic interaction between the fragile X mental retardation protein and the microRNA pathway.  Nat Neurosci. 2004;  7 113-117
  • 41 Jones-Rhoades M W, Bartel D P, Bartel B. MicroRNAs and their regulatory roles in plants.  Annu Rev Plant Biol. 2006;  57 19-53
  • 42 Doench J G, Sharp P A. Specificity of microRNA target selection in translational repression.  Genes Dev. 2004;  18 504-511
  • 43 Lewis B P, Burge C B, Bartel D P. Conserved seed pairing, often flanked by adenosines, indicates that thousands of human genes are microRNA targets.  Cell. 2005;  120 15-20
  • 44 Nielsen C B, Shomron N, Sandberg R, Hornstein E, Kitzman J, Burge C B. Determinants of targeting by endogenous and exogenous microRNAs and siRNAs.  RNA. 2007;  13 1894-1910
  • 45 Grun D, Wang Y L, Langenberger D, Gunsalus K C, Rajewsky N. microRNA target predictions across seven Drosophila species and comparison to mammalian targets.  PLOS Comput Biol. 2005;  1 66
  • 46 Kuhn D E, Martin M M, Feldman D S, Terry Jr A V, Nuovo G J, Elton T S. Experimental validation of miRNA targets.  Methods. 2008;  44 47-54
  • 47 Sood P, Krek A, Zavolan M, Macino G, Rajewsky N. Cell-type-specific signatures of microRNAs on target mRNA expression.  Proc Natl Acad Sci U S A. 2006;  103 2746-2751
  • 48 Giraldez A J, Mishima Y, Rihel J et al.. Zebrafish MiR-430 promotes deadenylation and clearance of maternal mRNAs.  Science. 2006;  312 75-79
  • 49 Stark A, Kheradpour P, Parts L et al.. Systematic discovery and characterization of fly microRNAs using 12 Drosophila genomes.  Genome Res. 2007;  17 1865-1879
  • 50 Hillier L W, Marth G T, Quinlan A R et al.. Whole-genome sequencing and variant discovery in C. elegans.  Nat Methods. 2008;  5 183-188
  • 51 Choi Y, Qin Y, Berger M F, Ballow D J, Bulyk M L, Rajkovic A. Microarray analyses of newborn mouse ovaries lacking Nobox.  Biol Reprod. 2007;  77 312-319
  • 52 Landgraf P, Rusu M, Sheridan R et al.. A mammalian microRNA expression atlas based on small RNA library sequencing.  Cell. 2007;  129 1401-1414
  • 53 Ro S, Song R, Park C, Zheng H, Sanders K M, Yan W. Cloning and expression profiling of small RNAs expressed in the mouse ovary.  RNA. 2007;  13 2366-2380
  • 54 Yang H, Kong W, He L et al.. MicroRNA expression profiling in human ovarian cancer: miR-214 induces cell survival and cisplatin resistance by targeting PTEN.  Cancer Res. 2008;  68 425-433
  • 55 Iorio M V, Visone R, Di Leva G et al.. MicroRNA signatures in human ovarian cancer.  Cancer Res. 2007;  67 8699-8707
  • 56 Pasquinelli A E, Reinhart B J, Slack F et al.. Conservation of the sequence and temporal expression of let-7 heterochronic regulatory RNA.  Nature. 2000;  408 86-89
  • 57 Yu F, Yao H, Zhu P et al.. let-7 regulates self renewal and tumorigenicity of breast cancer cells.  Cell. 2007;  131 1109-1123
  • 58 Park S M, Shell S, Radjabi A R et al.. Let-7 prevents early cancer progression by suppressing expression of the embryonic gene HMGA2.  Cell Cycle. 2007;  6 2585-2590
  • 59 Sampson V B, Rong N H, Han J et al.. MicroRNA let-7a down-regulates MYC and reverts MYC-induced growth in Burkitt lymphoma cells.  Cancer Res. 2007;  67 9762-9770
  • 60 John B, Enright A J, Aravin A, Tuschl T, Sander C, Marks D S. Human microRNA targets.  PLoS Biol. 2004;  2 1862-1879
  • 61 Pangas S A, Choi Y, Ballow D J et al.. Oogenesis requires germ cell-specific transcriptional regulators Sohlh1 and Lhx8.  Proc Natl Acad Sci U S A. 2006;  103 8090-8095
  • 62 Nakahara K, Kim K, Sciulli C, Dowd S R, Minden J S, Carthew R W. Targets of microRNA regulation in the Drosophila oocyte proteome.  Proc Natl Acad Sci U S A. 2005;  102 12023-12028
  • 63 Bernstein E, Kim S Y, Carmell M A et al.. Dicer is essential for mouse development.  Nat Genet. 2003;  35 215-217
  • 64 Su A I, Cooke M P, Ching K A et al.. Large-scale analysis of the human and mouse transcriptomes.  Proc Natl Acad Sci U S A. 2002;  99 4465-4470
  • 65 Murchison E P, Stein P, Xuan Z et al.. Critical roles for Dicer in the female germline.  Genes Dev. 2007;  21 682-693
  • 66 Tang F, Kaneda M, O'Carroll D et al.. Maternal microRNAs are essential for mouse zygotic development.  Genes Dev. 2007;  21 644-648
  • 67 Gallardo T, Shirley L, John G B, Castrillon D H. Generation of a germ cell-specific mouse transgenic Cre line, Vasa-Cre.  Genesis. 2007;  45 413-417
  • 68 Sullivan A K, Marcus M, Epstein M P et al.. Association of FMR1 repeat size with ovarian dysfunction.  Hum Reprod. 2005;  20 402-412
  • 69 Allen E G, Sullivan A K, Marcus M et al.. Examination of reproductive aging milestones among women who carry the FMR1 premutation.  Hum Reprod. 2007;  22 2142-2152
  • 70 Marozzi A, Vegetti W, Manfredini E et al.. Association between idiopathic premature ovarian failure and fragile X premutation.  Hum Reprod. 2000;  15 197-202
  • 71 Allingham-Hawkins D J, Babul-Hirji R, Chitayat D et al.. Fragile X premutation is a significant risk factor for premature ovarian failure: the International Collaborative POF in Fragile X study–preliminary data.  Am J Med Genet. 1999;  83 322-325
  • 72 Bardoni B, Mandel J L. Advances in understanding of fragile X pathogenesis and FMRP function, and in identification of X linked mental retardation genes.  Curr Opin Genet Dev. 2002;  12 284-293
  • 73 Ishizuka A, Siomi M C, Siomi H. A Drosophila fragile X protein interacts with components of RNAi and ribosomal proteins.  Genes Dev. 2002;  16 2497-2508
  • 74 Caudy A A, Myers M, Hannon G J, Hammond S M. Fragile X-related protein and VIG associate with the RNA interference machinery.  Genes Dev. 2002;  16 2491-2496
  • 75 Yang L, Duan R, Chen D, Wang J, Chen D, Jin P. Fragile X mental retardation protein modulates the fate of germline stem cells in Drosophila.  Hum Mol Genet. 2007;  16 1814-1820
  • 76 Zhang Y Q, Bailey A M, Matthies H J et al.. Drosophila fragile X-related gene regulates the MAP1B homolog Futsch to control synaptic structure and function.  Cell. 2001;  107 591-603
  • 77 Zhang Y Q, Matthies H J, Mancuso J et al.. The Drosophila fragile X-related gene regulates axoneme differentiation during spermatogenesis.  Dev Biol. 2004;  270 290-307
  • 78 Fmr1 knockout mice: a model to study fragile X mental retardation. The Dutch-Belgian Fragile X Consortium.  Cell. 1994;  78 23-33
  • 79 Entezam A, Biacsi R, Orrison B et al.. Regional FMRP deficits and large repeat expansions into the full mutation range in a new Fragile X premutation mouse model.  Gene. 2007;  395 125-134
  • 80 Jin P, Duan R, Qurashi A et al.. Pur alpha binds to rCGG repeats and modulates repeat-mediated neurodegeneration in a Drosophila model of fragile X tremor/ataxia syndrome.  Neuron. 2007;  55 556-564
  • 81 Sofola O A, Jin P, Qin Y et al.. RNA-binding proteins hnRNP A2/B1 and CUGBP1 suppress fragile X CGG premutation repeat-induced neurodegeneration in a Drosophila model of FXTAS.  Neuron. 2007;  55 565-571
  • 82 Bachner D, Manca A, Steinbach P et al.. Enhanced expression of the murine FMR1 gene during germ cell proliferation suggests a special function in both the male and the female gonad.  Hum Mol Genet. 1993;  2 2043-2050
  • 83 Rife M, Nadal A, Mila M, Willemsen R. Immunohistochemical FMRP studies in a full mutated female fetus.  Am J Med Genet A. 2004;  124 129-132

Aleksandar RajkovicM.D. Ph.D. 

Department of Obstetrics and Gynecology, Baylor College of Medicine

1709 Dryden Road, Suite 1100, Houston, TX 77030

Email: rajkovic@bcm.edu

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