Small RNA class transition from siRNA/piRNA to miRNA during pre-implantation mouse development

Recent studies showed that small interfering RNAs (siRNAs) and Piwi-interacting RNA (piRNA) in mammalian germ cells play important roles in retrotransposon silencing and gametogenesis. However, subsequent contribution of those small RNAs to early mammalian development remains poorly understood. We investigated the expression profiles of small RNAs in mouse metaphase II oocytes, 8–16-cell stage embryos, blastocysts and the pluripotent inner cell mass (ICM) using high-throughput pyrosequencing. Here, we show that during pre-implantation development a major small RNA class changes from retrotransposon-derived small RNAs containing siRNAs and piRNAs to zygotically synthesized microRNAs (miRNAs). Some siRNAs and piRNAs are transiently upregulated and directed against specific retrotransposon classes. We also identified miRNAs expression profiles characteristic of the ICM and trophectoderm (TE) cells. Taken together, our current study reveals a major reprogramming of functional small RNAs during early mouse development from oocyte to blastocyst.

[1]  Michael Q. Zhang,et al.  Critical roles for Dicer in the female germline. , 2007, Genes & development.

[2]  A. Rizzino,et al.  DNA microarray analyses of genes regulated during the differentiation of embryonic stem cells , 2000, Molecular reproduction and development.

[3]  Toshiaki Watanabe,et al.  Identification and characterization of two novel classes of small RNAs in the mouse germline: retrotransposon-derived siRNAs in oocytes and germline small RNAs in testes. , 2006, Genes & development.

[4]  G. Hannon,et al.  RNAi and expression of retrotransposons MuERV-L and IAP in preimplantation mouse embryos. , 2004, Developmental biology.

[5]  G. Pan,et al.  MicroRNA-145 Regulates OCT4, SOX2, and KLF4 and Represses Pluripotency in Human Embryonic Stem Cells , 2009, Cell.

[6]  Megan F. Cole,et al.  Connecting microRNA Genes to the Core Transcriptional Regulatory Circuitry of Embryonic Stem Cells , 2008, Cell.

[7]  W. Deng,et al.  miwi, a murine homolog of piwi, encodes a cytoplasmic protein essential for spermatogenesis. , 2002, Developmental cell.

[8]  M. Zernicka-Goetz,et al.  Efficient delivery of dsRNA into zona‐enclosed mouse oocytes and preimplantation embryos by electroporation , 2002, Genesis.

[9]  Takashi Hiiragi,et al.  Stochastic patterning in the mouse pre-implantation embryo , 2007, Development.

[10]  F. Tang,et al.  Maternal microRNAs are essential for mouse zygotic development. , 2007, Genes & development.

[11]  N. Lau,et al.  Characterization of the piRNA Complex from Rat Testes , 2006, Science.

[12]  D. Solter,et al.  Immunosurgery of mouse blastocyst. , 1975, Proceedings of the National Academy of Sciences of the United States of America.

[13]  C. Sander,et al.  A novel class of small RNAs bind to MILI protein in mouse testes , 2006, Nature.

[14]  R. Schultz,et al.  RNA transcript profiling during zygotic gene activation in the preimplantation mouse embryo. , 2005, Developmental biology.

[15]  Kenichiro Hata,et al.  DNA methylation of retrotransposon genes is regulated by Piwi family members MILI and MIWI2 in murine fetal testes. , 2008, Genes & development.

[16]  A. Schier,et al.  Target Protectors Reveal Dampening and Balancing of Nodal Agonist and Antagonist by miR-430 , 2007, Science.

[17]  D. Bartel.  MicroRNAs Genomics, Biogenesis, Mechanism, and Function , 2004, Cell.

[18]  M. Murakami,et al.  The Homeoprotein Nanog Is Required for Maintenance of Pluripotency in Mouse Epiblast and ES Cells , 2003, Cell.

[19]  D. Melton,et al.  "Stemness": Transcriptional Profiling of Embryonic and Adult Stem Cells , 2002, Science.

[20]  S. Elledge,et al.  Dicer is essential for mouse development , 2003, Nature Genetics.

[21]  Ryo Matoba,et al.  High-throughput screen for genes predominantly expressed in the ICM of mouse blastocysts by whole mount in situ hybridization. , 2006, Gene expression patterns : GEP.

[22]  Anton J. Enright,et al.  Zebrafish MiR-430 Promotes Deadenylation and Clearance of Maternal mRNAs , 2006, Science.

[23]  A. Sharov,et al.  Dynamics of global gene expression changes during mouse preimplantation development. , 2004, Developmental cell.

[24]  Janet Rossant,et al.  Blastocyst lineage formation, early embryonic asymmetries and axis patterning in the mouse , 2009, Development.

[25]  W. Reik,et al.  Epigenetic Reprogramming in Mammalian Development , 2001, Science.

[26]  Robert Blelloch,et al.  Mouse ES cells express endogenous shRNAs, siRNAs, and other Microprocessor-independent, Dicer-dependent small RNAs. , 2008, Genes & development.

[27]  Janet Rossant,et al.  Cdx2 is required for correct cell fate specification and differentiation of trophectoderm in the mouse blastocyst , 2005, Development.

[28]  W. Reik,et al.  Epigenetic reprogramming in mammals. , 2005, Human molecular genetics.

[29]  Ravi Sachidanandam,et al.  A germline-specific class of small RNAs binds mammalian Piwi proteins , 2006, Nature.

[30]  P. Sharp,et al.  Embryonic stem cell-specific MicroRNAs. , 2003, Developmental cell.

[31]  Yoichi Matsuda,et al.  Mili, a mammalian member of piwi family gene, is essential for spermatogenesis , 2004, Development.

[32]  H. Schöler,et al.  Oct-4 transcription factor is differentially expressed in the mouse embryo during establishment of the first two extraembryonic cell lineages involved in implantation. , 1994, Developmental biology.

[33]  Gene W Yeo,et al.  RNA sequence analysis defines Dicer's role in mouse embryonic stem cells , 2007, Proceedings of the National Academy of Sciences.

[34]  Oliver H. Tam,et al.  Pseudogene-derived small interfering RNAs regulate gene expression in mouse oocytes , 2008, Nature.

[35]  A. Caudy,et al.  Role for a bidentate ribonuclease in the initiation step of RNA interference , 2001 .

[36]  N. D. Clarke,et al.  Integration of External Signaling Pathways with the Core Transcriptional Network in Embryonic Stem Cells , 2008, Cell.

[37]  Y. Sakaki,et al.  Endogenous siRNAs from naturally formed dsRNAs regulate transcripts in mouse oocytes , 2008, Nature.

[38]  C. Bult,et al.  Systems biology of the 2-cell mouse embryo , 2004, Cytogenetic and Genome Research.

[39]  T. Tuschl,et al.  Cloning of Small RNA Molecules , 2003, Current protocols in molecular biology.

[40]  G. Hannon,et al.  MIWI2 is essential for spermatogenesis and repression of transposons in the mouse male germline. , 2007, Developmental cell.

[41]  A. Evsikov,et al.  Retrotransposons regulate host genes in mouse oocytes and preimplantation embryos. , 2004, Developmental cell.

[42]  Edwin Cuppen,et al.  Diversity of microRNAs in human and chimpanzee brain , 2006, Nature Genetics.

[43]  W. Dean,et al.  Epigenetic reprogramming during early development in mammals. , 2004, Reproduction.

[44]  Sheng Zhong,et al.  A core Klf circuitry regulates self-renewal of embryonic stem cells , 2008, Nature Cell Biology.

[45]  L. Lim,et al.  An Abundant Class of Tiny RNAs with Probable Regulatory Roles in Caenorhabditis elegans , 2001, Science.

[46]  Uyen Tran,et al.  MicroRNA control of Nodal signalling , 2007, Nature.

[47]  G. Bell,et al.  Functional studies of signaling pathways in peri-implantation development of the mouse embryo by RNAi , 2005, BMC Developmental Biology.