Selective stabilization of mammalian microRNAs by 3' adenylation mediated by the cytoplasmic poly(A) polymerase GLD-2.

The steady-state levels of microRNAs (miRNAs) and their activities are regulated by the post-transcriptional processes. It is known that 3' ends of several miRNAs undergo post-dicing adenylation or uridylation. We isolated the liver-specific miR-122 from human hepatocytes and mouse livers. Direct analysis by mass spectrometry revealed that one variant of miR-122 has a 3'-terminal adenosine that is introduced after processing by Dicer. We identified GLD-2, which is a regulatory cytoplasmic poly(A) polymerase, as responsible for the 3'-terminal adenylation of miR-122 after unwinding of the miR-122/miR-122* duplex. In livers from GLD-2-null mice, the steady-state level of the mature form of miR-122 was specifically lower than in heterozygous mice, whereas no reduction of pre-miR-122 was observed, demonstrating that 3'-terminal adenylation by GLD-2 is required for the selective stabilization of miR-122 in the liver.

[1]  C. Joo,et al.  Lin28 mediates the terminal uridylation of let-7 precursor MicroRNA. , 2008, Molecular cell.

[2]  M. Wickens,et al.  GLD2 poly(A) polymerase is required for long-term memory , 2008, Proceedings of the National Academy of Sciences.

[3]  Xuemei Chen,et al.  Degradation of microRNAs by a Family of Exoribonucleases in Arabidopsis , 2008, Science.

[4]  L. Smirnova,et al.  A feedback loop comprising lin-28 and let-7 controls pre-let-7 maturation during neural stem-cell commitment , 2008, Nature Cell Biology.

[5]  Kiyoshi Asai,et al.  Characterization of endogenous human Argonautes and their miRNA partners in RNA silencing , 2008, Proceedings of the National Academy of Sciences.

[6]  T. Nakanishi,et al.  Non-canonical poly(A) polymerase in mammalian gametogenesis. , 2008, Biochimica et biophysica acta.

[7]  M. Wickens,et al.  Multifunctional deadenylase complexes diversify mRNA control , 2008, Nature Reviews Molecular Cell Biology.

[8]  Vanessa L. Horner,et al.  Wispy, the Drosophila Homolog of GLD-2, Is Required During Oogenesis and Egg Activation , 2008, Genetics.

[9]  A. Silahtaroglu,et al.  Antagonism of microRNA-122 in mice by systemically administered LNA-antimiR leads to up-regulation of a large set of predicted target mRNAs in the liver , 2007, Nucleic acids research.

[10]  Stijn van Dongen,et al.  miRBase: tools for microRNA genomics , 2007, Nucleic Acids Res..

[11]  M. Kimura,et al.  Disruption of mouse poly(A) polymerase mGLD-2 does not alter polyadenylation status in oocytes and somatic cells. , 2007, Biochemical and biophysical research communications.

[12]  Georges Martin,et al.  RNA-specific ribonucleotidyl transferases. , 2007, RNA.

[13]  C. Sander,et al.  A Mammalian microRNA Expression Atlas Based on Small RNA Library Sequencing , 2007, Cell.

[14]  J. Richter,et al.  CPEB: a life in translation. , 2007, Trends in biochemical sciences.

[15]  M. Wickens,et al.  A family of poly(U) polymerases. , 2007, RNA.

[16]  H. Ueda,et al.  The 3′ termini of mouse Piwi-interacting RNAs are 2′-O-methylated , 2007, Nature Structural &Molecular Biology.

[17]  C. Norbury,et al.  Efficient RNA Polyuridylation by Noncanonical Poly(A) Polymerases , 2007, Molecular and Cellular Biology.

[18]  Lena Smirnova,et al.  The FASEB Journal • Research Communication Post-transcriptional regulation of the let-7 microRNA during neural cell specification , 2022 .

[19]  T. Katoh,et al.  Specific residues at every third position of siRNA shape its efficient RNAi activity , 2007, Nucleic acids research.

[20]  Tsutomu Suzuki,et al.  Automated parallel isolation of multiple species of non-coding RNAs by the reciprocal circulating chromatography method , 2007, Nucleic acids research.

[21]  Tsutomu Suzuki,et al.  Mass spectrometric identification and characterization of RNA-modifying enzymes. , 2007, Methods in enzymology.

[22]  Christopher M. Player,et al.  Large-Scale Sequencing Reveals 21U-RNAs and Additional MicroRNAs and Endogenous siRNAs in C. elegans , 2006, Cell.

[23]  Joel S Parker,et al.  Extensive post-transcriptional regulation of microRNAs and its implications for cancer. , 2006, Genes & development.

[24]  G. Obernosterer,et al.  Post-transcriptional regulation of microRNA expression. , 2006, RNA.

[25]  W. Filipowicz,et al.  Relief of microRNA-Mediated Translational Repression in Human Cells Subjected to Stress , 2006, Cell.

[26]  Masahiro Sato,et al.  The expression profile of microRNAs in mouse embryos , 2006, Nucleic acids research.

[27]  Mark Graham,et al.  miR-122 regulation of lipid metabolism revealed by in vivo antisense targeting. , 2006, Cell metabolism.

[28]  T. Nakanishi,et al.  Possible role of mouse poly(A) polymerase mGLD-2 during oocyte maturation. , 2006, Developmental biology.

[29]  P. Seeburg,et al.  Modulation of microRNA processing and expression through RNA editing by ADAR deaminases , 2006, Nature Structural &Molecular Biology.

[30]  N. Rajewsky,et al.  Silencing of microRNAs in vivo with ‘antagomirs’ , 2005, Nature.

[31]  P. Sarnow,et al.  Modulation of Hepatitis C Virus RNA Abundance by a Liver-Specific MicroRNA , 2005, Science.

[32]  Xuemei Chen,et al.  Methylation Protects miRNAs and siRNAs from a 3′-End Uridylation Activity in Arabidopsis , 2005, Current Biology.

[33]  M. Wickens,et al.  Vertebrate GLD2 poly(A) polymerases in the germline and the brain. , 2005, RNA.

[34]  V. Kim MicroRNA biogenesis: coordinated cropping and dicing , 2005, Nature Reviews Molecular Cell Biology.

[35]  Xuemei Chen,et al.  Methylation as a Crucial Step in Plant microRNA Biogenesis , 2005, Science.

[36]  K. Ryan,et al.  Symplekin and xGLD-2 Are Required for CPEB-Mediated Cytoplasmic Polyadenylation , 2004, Cell.

[37]  H. Goodman,et al.  Uridine Addition After MicroRNA-Directed Cleavage , 2004, Science.

[38]  C. Sander,et al.  miR-122, a Mammalian Liver-Specific microRNA, is Processed from hcr mRNA and MayDownregulate the High Affinity Cationic Amino Acid Transporter CAT-1 , 2004, RNA biology.

[39]  S. Moon,et al.  Human embryonic stem cells express a unique set of microRNAs. , 2004, Developmental biology.

[40]  M. Wickens,et al.  A regulatory cytoplasmic poly(A) polymerase in Caenorhabditis elegans , 2002, Nature.

[41]  A. Carr,et al.  Cytoplasmic poly(A) polymerases mediate cellular responses to S phase arrest , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[42]  J. Yates,et al.  Cid13 Is a Cytoplasmic Poly(A) Polymerase that Regulates Ribonucleotide Reductase mRNA , 2002, Cell.

[43]  R. Reddy,et al.  The 3' end formation in small RNAs. , 2002, Gene expression.

[44]  R. Méndez,et al.  Translational control by CPEB: a means to the end , 2001, Nature Reviews Molecular Cell Biology.

[45]  K. Sinha,et al.  Purification, Characterization, and Cloning of the cDNA of Human Signal Recognition Particle RNA 3′-Adenylating Enzyme* , 2001, The Journal of Biological Chemistry.

[46]  Yahua Chen,et al.  Effect of 3' terminal adenylic acid residue on the uridylation of human small RNAs in vitro and in frog oocytes. , 2000, RNA.

[47]  Gary L. Glish,et al.  Tandem Mass Spectrometry of Small, Multiply Charged Oligonucleotides , 1992, Journal of the American Society for Mass Spectrometry.

[48]  Vlad I. Morariu,et al.  Expression , 2015, Principles of Molecular Virology.