PAPD5-mediated 3′ adenylation and subsequent degradation of miR-21 is disrupted in proliferative disease

Proceedings of the National Academy of Sciences of the United States of America

Volumn 111, Issue 31, 2014, Pages 11467-11472

  Boele, Joost ^a,b   Persson, Helena ^c,d   Shin, Jay W ^a   Ishizu, Yuri ^a   Newie, Inga S ^d   Søkilde, Rolf ^d   Hawkins, Shannon M ^e   Coarfa, Cristian ^e   Ikeda, Kazuhiro ^f   Takayama, Ken Ichi ^g   Horie Inoue, Kuniko ^f   Ando, Yoshinari ^a,h   Burroughs, A Maxwell ^a,i   Sasaki, Chihiro ^a   Suzuki, Chizuru ^a   Sakai, Mizuho ^a   Aoki, Shintaro ^a   Ogawa, Ayumi ^a   Hasegawa, Akira ^a   Lizio, Marina ^a   Kaida, Kaoru ^a   Teusink, Bas ^b   Carninci, Piero ^a   Suzuki, Harukazu ^a   Inoue, Satoshi ^f,g   Gunaratne, Preethi H ^e,j   Rovira, Carlos ^d   Hayashizaki, Yoshihide ^a   De Hoon, Michiel J L ^a   more..

^a RIKEN   (Japan)

^b AMSTERDAM INSTITUTE FOR MOLECULES   (Netherlands)

^c KAROLINSKA INSTITUTE   (Sweden)

^d LUND UNIVERSITY   (Sweden)

^e BAYLOR COLLEGE OF MEDICINE   (United States)

^f SAITAMA MEDICAL UNIVERSITY   (Japan)

^g UNIVERSITY OF TOKYO   (Japan)

^h JOHNS HOPKINS BLOOMBERG SCHOOL OF PUBLIC HEALTH   (United States)

ⁱ NATIONAL INSTITUTES OF HEALTH   (United States)

^j University of Houston   (United States)

more..

Author keywords

microRNA processing; Nucleotidyl transferase

Indexed keywords

DICER1 ENZYME; ESTERASE; EXORIBONUCLEASE; MICRORNA 21; PAPD5 PROTEIN; POLYNUCLEOTIDE ADENYLYLTRANSFERASE; UNCLASSIFIED DRUG;

ADENYLATION; ARTICLE; GENE DISRUPTION; MCF 7 CELL LINE; MICROARRAY ANALYSIS; NEOPLASM; PRIORITY JOURNAL; PROTEIN CLEAVAGE; PSORIASIS; RECEPTOR DOWN REGULATION; RNA DEGRADATION; RNA SEQUENCE;

MICRORNA PROCESSING; NUCLEOTIDYL TRANSFERASE;

ADENINE; BASE SEQUENCE; CYTOSINE; EXORIBONUCLEASES; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, NEOPLASTIC; GENE KNOCKDOWN TECHNIQUES; HIGH-THROUGHPUT NUCLEOTIDE SEQUENCING; HUMANS; MCF-7 CELLS; MICRORNAS; MODELS, BIOLOGICAL; MOLECULAR SEQUENCE DATA; NEOPLASMS; NUCLEIC ACID CONFORMATION; PROTEIN ISOFORMS; RIBONUCLEASE III; RNA NUCLEOTIDYLTRANSFERASES; RNA STABILITY;

EID: 84905656796     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1317751111     Document Type: Article

References (60)

1. Lee RC, Feinbaum RL, Ambros V (1993) The C. elegans heterochronic gene lin-4 encodes small RNAs with antisense complementarity to lin-14. Cell 75(5):843-854. (Pubitemid 24014542)
2. Lee LW, et al. (2010) Complexity of the microRNA repertoire revealed by next-generation sequencing. RNA 16(11):2170-2180.
3. Winter J, Jung S, Keller S, Gregory RI, Diederichs S (2009) Many roads to maturity: MicroRNA biogenesis pathways and their regulation. Nat Cell Biol 11(3):228-234.
4. Hutvagner G, Simard MJ (2008) Argonaute proteins: Key players in RNA silencing. Nat Rev Mol Cell Biol 9(1):22-32.
5. Kawahara Y, Zinshteyn B, Chendrimada TP, Shiekhattar R, Nishikura K (2007) RNA editing of the microRNA-151 precursor blocks cleavage by the Dicer-TRBP complex. EMBO Rep 8(8):763-769. (Pubitemid 47202456)
6. Kawahara Y, et al. (2008) Frequency and fate of microRNA editing in human brain. Nucleic Acids Res 36(16):5270-5280.
7. Viswanathan SR, Daley GQ, Gregory RI (2008) Selective blockade of microRNA processing by Lin28. Science 320(5872):97-100. (Pubitemid 351490762)
8. Heo I, et al. (2008) Lin28 mediates the terminal uridylation of let-7 precursor Micro-RNA. Mol Cell 32(2):276-284.
9. Heo I, et al. (2009) TUT4 in concert with Lin28 suppresses microRNA biogenesis through pre-microRNA uridylation. Cell 138(4):696-708.
10. Hagan JP, Piskounova E, Gregory RI (2009) Lin28 recruits the TUTase Zcchc11 to inhibit let-7 maturation in mouse embryonic stem cells. Nat Struct Mol Biol 16(10):1021-1025.
11. Landgraf P, et al. (2007) A mammalian microRNA expression atlas based on small RNA library sequencing. Cell 129(7):1401-1414. (Pubitemid 46970709)
12. Kuchenbauer F, et al. (2008) In-depth characterization of the microRNA transcriptome in a leukemia progression model. Genome Res 18(11):1787-1797.
13. Morin RD, et al. (2008) Application of massively parallel sequencing to microRNA profiling and discovery in human embryonic stem cells. Genome Res 18(4):610-621. (Pubitemid 351482785)
14. Starega-Roslan J, et al. (2011) Structural basis of microRNA length variety. Nucleic Acids Res 39(1):257-268.
15. Burroughs AM, et al. (2011) Deep-sequencing of human Argonaute-associated small RNAs provides insight into miRNA sorting and reveals Argonaute association with RNA fragments of diverse origin. RNA Biol 8(1):158-177.
16. Azuma-Mukai A, et al. (2008) Characterization of endogenous human Argonautes and their miRNA partners in RNA silencing. Proc Natl Acad Sci USA 105(23):7964-7969. (Pubitemid 351904690)
17. Burroughs AM, et al. (2010) A comprehensive survey of 3′ animal miRNA modification events and a possible role for 3′ adenylation in modulating miRNA targeting effectiveness. Genome Res 20(10):1398-1410.
18. Wyman SK, et al. (2011) Post-transcriptional generation of miRNA variants by multiple nucleotidyl transferases contributes to miRNA transcriptome complexity. Genome Res 21(9):1450-1461.
19. Katoh T, et al. (2009) Selective stabilization of mammalian microRNAs by 3′ adenylation mediated by the cytoplasmic poly(A) polymerase GLD-2. Genes Dev 23(4):433-438.
20. Krol J, Loedige I, Filipowicz W (2010) The widespread regulation of microRNA biogenesis, function and decay. Nat Rev Genet 11(9):597-610.
21. Yang CH, Yue J, Pfeffer SR, Handorf CR, Pfeffer LM(2011) MicroRNA miR-21 regulates the metastatic behavior of B16 melanoma cells. J Biol Chem 286(45):39172-39178.
22. Jazbutyte V, Thum T (2010) MicroRNA-21: From cancer to cardiovascular disease. Curr Drug Targets 11(8):926-935.
23. Medina PP, Nolde M, Slack FJ (2010) OncomiR addiction in an in vivo model of microRNA-21-induced pre-B-cell lymphoma. Nature 467(7311):86-90.
24. Cheng Y, Zhang C (2010) MicroRNA-21 in cardiovascular disease. J Cardiovasc Transl Res 3(3):251-255.
25. Joyce CE, et al. (2011) Deep sequencing of small RNAs from human skin reveals major alterations in the psoriasis miRNAome. Hum Mol Genet 20(20):4025-4040.
26. Liu M, et al. (2009) Regulation of the cell cycle gene, BTG2, by miR-21 in human laryngeal carcinoma. Cell Res 19(7):828-837.
27. Niu J, et al. (2012) DNA damage induces NF-κB-dependent microRNA-21 up-regulation and promotes breast cancer cell invasion. J Biol Chem 287(26):21783-21795.
28. The Cancer Genome Atlas. Available at http://cancergenome.nih.gov. Accessed August 29, 2013.
29. Burns DM, D'Ambrogio A, Nottrott S, Richter JD (2011) CPEB and two poly(A) polymerases control miR-122 stability and p53 mRNA translation. Nature 473(7345):105-108.
30. Kozomara A, Griffiths-Jones S (2014) miRBase: Annotating high confidence micro-RNAs using deep sequencing data. Nucleic Acids Res 42(Database issue):D68-D73.
31. Taft RJ, et al. (2009) Tiny RNAs associated with transcription start sites in animals. Nat Genet 41(5):572-578.
32. Lee HY, Doudna JA (2012) TRBP alters human precursor microRNA processing in vitro. RNA 18(11):2012-2019.
33. Ando Y, et al. (2011) Two-step cleavage of hairpin RNA with 5′ overhangs by human DICER. BMC Mol Biol 12:6.
34. Zhang H, Kolb FA, Jaskiewicz L, Westhof E, Filipowicz W (2004) Single processing center models for human Dicer and bacterial RNase III. Cell 118(1):57-68. (Pubitemid 38902814)
35. Ameres SL, et al. (2010) Target RNA-directed trimming and tailing of small silencing RNAs. Science 328(5985):1534-1539.
36. Rammelt C, Bilen B, Zavolan M, Keller W (2011) PAPD5, a noncanonical poly(A) polymerase with an unusual RNA-binding motif. RNA 17(9):1737-1746.
37. Hafner M, et al. (2010) Transcriptome-wide identification of RNA-binding protein and microRNA target sites by PAR-CLIP. Cell 141(1):129-141.
38. Berndt H, et al. (2012) Maturation of mammalian H/ACA box snoRNAs: PAPD5-dependent adenylation and PARN-dependent trimming. RNA 18(5):958-972.
39. Virtanen A, Henriksson N, Nilsson P, Nissbeck M (2013) Poly(A)-specific ribonuclease (PARN): An allosterically regulated, processive and mRNA cap-interacting deadenylase. Crit Rev Biochem Mol Biol 48(2):192-209.
40. Friedman RC, Farh KK, Burge CB, Bartel DP (2009) Most mammalian mRNAs are conserved targets of microRNAs. Genome Res 19(1):92-105.
41. Lewis BP, Shih IH, Jones-Rhoades MW, Bartel DP, Burge CB (2003) Prediction of mammalian microRNA targets. Cell 115(7):787-798. (Pubitemid 38058492)
42. Roberson ED, Bowcock AM (2010) Psoriasis genetics: Breaking the barrier. Trends Genet 26(9):415-423.
43. Liu N, et al. (2011) The exoribonuclease Nibbler controls 3′ end processing of micro-RNAs in Drosophila. Curr Biol 21(22):1888-1893.
44. Han BW, Hung JH, Weng Z, Zamore PD, Ameres SL (2011) The 3′-to-5′ exoribonuclease Nibbler shapes the 3′ ends of microRNAs bound to Drosophila Argonaute1. Curr Biol 21(22):1878-1887.
45. Burroughs AM, Kawano M, Ando Y, Daub CO, Hayashizaki Y (2012) pre-miRNA profiles obtained through application of locked nucleic acids and deep sequencing reveals complex 5′/3′ arm variation including concomitant cleavage and polyuridylation patterns. Nucleic Acids Res 40(4):1424-1437.
46. Lee Y, et al. (2003) The nuclear RNase III Drosha initiates microRNA processing. Nature 425(6956):415-419. (Pubitemid 37187272)
47. Gregory RI, et al. (2004) The microprocessor complex mediates the genesis of microRNAs. Nature 432(7014):235-240. (Pubitemid 39545855)
48. Pedersen IM, et al. (2007) Interferon modulation of cellular microRNAs as an antiviral mechanism. Nature 449(7164):919-922. (Pubitemid 47598616)
49. Marcinowski L, et al. (2012) Degradation of cellular mir-27 by a novel, highly abundant viral transcript is important for efficient virus replication in vivo. PLoS Pathog 8(2):e1002510.
50. Yoda M, et al. (2013) Poly(A)-specific ribonuclease mediates 3′-end trimming of Argonaute2-cleaved precursor microRNAs. Cell Reports 5(3):715-726.
51. Devany E, Zhang X, Park JY, Tian B, Kleiman FE (2013) Positive and negative feedback loops in the p53 and mRNA 3′ processing pathways. Proc Natl Acad Sci USA 110(9):3351-3356.
52. Fu Y, et al. (2011) Identification and differential expression of microRNAs during metamorphosis of the Japanese flounder (Paralichthys olivaceus). PLoS ONE 6(7):e22957.
53. Robinson MD, McCarthy DJ, Smyth GK (2010) edgeR: A Bioconductor package for differential expression analysis of digital gene expression data. Bioinformatics 26(1):139-140.
54. Wilks SS (1938) The large-sample distribution of the likelihood ratio for testing composite hypotheses. Ann Math Stat 9(1):60-62.
55. Zuker M (2003) Mfold web server for nucleic acid folding and hybridization prediction. Nucleic Acids Res 31(13):3406-3415.
56. Hanahan D, Weinberg RA (2011) Hallmarks of cancer: The next generation. Cell 144(5):646-674.
57. Meng F, et al. (2007) MicroRNA-21 regulates expression of the PTEN tumor suppressor gene in human hepatocellular cancer. Gastroenterology 133(2):647-658. (Pubitemid 47187346)
58. Asangani IA, et al. (2008) MicroRNA-21 (miR-21) post-transcriptionally downregulates tumor suppressor Pdcd4 and stimulates invasion, intravasation and metastasis in colorectal cancer. Oncogene 27(15):2128-2136. (Pubitemid 351485639)
59. Thum T, et al. (2008) MicroRNA-21 contributes to myocardial disease by stimulating MAP kinase signalling in fibroblasts. Nature 456(7224):980-984.
60. Zhu S, et al. (2008) MicroRNA-21 targets tumor suppressor genes in invasion and metastasis. Cell Res 18(3):350-359. (Pubitemid 351333899)