A comprehensive survey of 3′ animal miRNA modification events and a possible role for 3′ adenylation in modulating miRNA targeting effectiveness

Genome Research

Volumn 20, Issue 10, 2010, Pages 1398-1410

  Burroughs, A Maxwell ^a   Ando, Yoshinari ^a   De Hoon, Michiel J L ^a   Tomaru, Yasuhiro ^a,b   Nishibu, Takahiro ^c   Ukekawa, Ryo ^c   Funakoshi, Taku ^c   Kurokawa, Tsutomu ^c   Suzuki, Harukazu ^a   Hayashizaki, Yoshihide ^a,b   Daub, Carsten O ^a  

^a RIKEN YOKOHAMA INSTITUTE   (Japan)

^b YOKOHAMA CITY UNIVERSITY   (Japan)

^c FUJIFILM Wako Pure Chemical Corporation   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

ADENINE; ARGONAUTE 1 PROTEIN; ARGONAUTE 2 PROTEIN; ARGONAUTE 3 PROTEIN; ARGONAUTE PROTEIN; MICRORNA; NUCLEOTIDYLTRANSFERASE; PAPD4 PROTEIN; UNCLASSIFIED DRUG;

3' UNTRANSLATED REGION; ADENYLATION; ANIMAL CELL; ARTICLE; CHICKEN; CONTROLLED STUDY; DNA MODIFICATION; DROSOPHILA; GENE LOCUS; GENE SILENCING; GENE TARGETING; HUMAN; HUMAN CELL; IMMUNOPRECIPITATION; MOUSE; NONHUMAN; PRIORITY JOURNAL; RNA SEQUENCE; RNA STABILITY; SEQUENCE ANALYSIS;

3' UNTRANSLATED REGIONS; ADENINE; ANIMALS; CELL LINE; EUKARYOTIC INITIATION FACTOR-2; EUKARYOTIC INITIATION FACTORS; HUMANS; MICE; MICRORNAS; MONOCYTES; MRNA CLEAVAGE AND POLYADENYLATION FACTORS; NUCLEOTIDYLTRANSFERASES; RNA STABILITY;

ANIMALIA; VERTEBRATA;

EID: 78649255480     PISSN: 10889051     EISSN: 15495469     Source Type: Journal    
DOI: 10.1101/gr.106054.110     Document Type: Article

References (58)

1. Anantharaman V, Koonin EV, Aravind L. 2002. Comparative genomics and evolution of proteins involved in RNA metabolism. Nucleic Acids Res 30: 1427-1464. (Pubitemid 34679722)
2. Aravind L, Koonin EV. 1999. DNA polymerase beta-like nucleotidyltransferase superfamily: identification of three new families, classification and evolutionary history. Nucleic Acids Res 27: 1609-1618.
3. Barnard DC, Ryan K, Manley JL, Richter JD. 2004. Symplekin and xGLD-2 are required for CPEB-mediated cytoplasmic polyadenylation. Cell 119: 641-651.
4. Benoit P, Papin C, Kwak JE, Wickens M, Simonelig M. 2008. PAP- and GLD-2- type poly(A) polymerases are required sequentially in cytoplasmic polyadenylation and oogenesis in Drosophila. Development 135: 1969-1979.
5. Cimmino A, Calin GA, Fabbri M, Iorio MV, Ferracin M, Shimizu M, Wojcik SE, Aqeilan RI, Zupo S, Dono M, et al. 2005. miR-15 and miR-16 induce apoptosis by targeting BCL2. Proc Natl Acad Sci 102: 13944-13949.
6. De Hoon MJ, Taft RJ, Hashimoto T, Kanamori-Katayama M, Kawaji H, Kawano M, Kishima M, Lassmann T, Faulkner GJ, Mattick JS, et al. 2010. Cross-mapping and the identification of editing sites in mature microRNAs in high-throughput sequencing libraries. Genome Res 20: 257-264.
7. The FANTOM Consortium and the Riken Omics Science Center. 2009. The transcriptional network that controls growth arrest and differentiation in a human myeloid leukemia cell line. Nat Genet 41: 553-562.
8. Forstemann K, Horwich MD, Wee L, Tomari Y, Zamore PD. 2007. Drosophila microRNAs are sorted into functionally distinct argonaute complexes after production by dicer-1. Cell 130: 287-297. (Pubitemid 47086327)
9. Ghildiyal M, Xu J, Seitz H, Weng Z, Zamore PD. 2010. Sorting of Drosophila small silencing RNAs partitions microRNA* strands into the RNA interference pathway. RNA 16: 43-56.
10. Glazov EA, Cottee PA, Barris WC, Moore RJ, Dalrymple BP, Tizard ML. 2008. A microRNA catalog of the developing chicken embryo identified by a deep sequencing approach. Genome Res 18: 957-964.
11. Griffiths-Jones S, Saini HK, van Dongen S, Enright AJ. 2008. miRBase: Tools for microRNA genomics. Nucleic Acids Res 36: D154-D158.
12. Grimson A, Srivastava M, Fahey B, Woodcroft BJ, Chiang HR, King N, Degnan BM, Rokhsar DS, Bartel DP. 2008. Early origins and evolution of microRNAs and Piwi-interacting RNAs in animals. Nature 455: 1193-1197.
13. 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: 1021-1025.
14. Han J, Lee Y, Yeom KH, Nam JW, Heo I, Rhee JK, Sohn SY, Cho Y, Zhang BT, Kim VN. 2006. Molecular basis for the recognition of primary microRNAs by the Drosha-DGCR8 complex. Cell 125: 887-901.
15. Heo I, Joo C, Kim YK, Ha M, Yoon MJ, Cho J, Yeom KH, Han J, Kim VN. 2009. TUT4 in concert with Lin28 suppresses microRNA biogenesis through pre-microRNA uridylation. Cell 138: 696-708.
16. Hock J, Meister G. 2008. The Argonaute protein family. Genome Biol 9: 210.
17. Hutvagner G, Simard MJ. 2008. Argonaute proteins: Key players in RNA silencing. Nat Rev Mol Cell Biol 9: 22-32.
18. Ivanovska I, Ball AS, Diaz RL, Magnus JF, Kibukawa M, Schelter JM, Kobayashi SV, Lim L, Burchard J, Jackson AL, et al. 2008. MicroRNAs in the miR-106b family regulate p21/CDKN1A and promote cell cycle progression. Mol Cell Biol 28: 2167-2174.
19. Jones MR, Quinton LJ, Blahna MT, Neilson JR, Fu S, Ivanov AR, Wolf DA, Mizgerd JP. 2009. Zcchc11-dependent uridylation of microRNA directs cytokine expression. Nat Cell Biol 11: 1157-1163.
20. Kai ZS, Pasquinelli AE. 2010. MicroRNA assassins: Factors that regulate the disappearance of miRNAs. Nat Struct Mol Biol 17: 5-10.
21. Katoh T, Sakaguchi Y, Miyauchi K, Suzuki T, Kashiwabara S, Baba T. 2009. Selective stabilization of mammalian microRNAs by 3′ adenylation mediated by the cytoplasmic poly(A) polymerase GLD-2. Genes Dev 23: 433-438.
22. Kawamata T, Seitz H, Tomari Y. 2009. Structural determinants ofmiRNAs for RISC loading and slicer-independent unwinding. Nat Struct Mol Biol 16: 953-960.
23. Koralov SB, Muljo SA, Galler GR, Krek A, Chakraborty T, Kanellopoulou C, Jensen K, Cobb BS, Merkenschlager M, Rajewsky N, et al. 2008. Dicer ablation affects antibody diversity and cell survival in the B lymphocyte lineage. Cell 132: 860-874.
24. Kwak JE, Drier E, Barbee SA, Ramaswami M, Yin JC, Wickens M. 2008. GLD2 poly(A) polymerase is required for long-term memory. Proc Natl Acad Sci 105: 14644-14649.
25. Lal A, Navarro F, Maher CA, Maliszewski LE, Yan N, O'Day E, Chowdhury D, Dykxhoorn DM, Tsai P, Hofmann O, et al. 2009. miR-24 Inhibits cell proliferation by targeting E2F2, MYC, and other cell-cycle genes via binding to "seedless" 39 UTR microRNA recognition elements. Mol Cell 35: 610-625.
26. Landgraf P, Rusu M, Sheridan R, Sewer A, Iovino N, Aravin A, Pfeffer S, Rice A, Kamphorst AO, Landthaler M, et al. 2007. A mammalian microRNA expression atlas based on small RNA library sequencing. Cell 129: 1401-1414.
27. Lassmann T, Hayashizaki Y, Daub CO. 2009. TagDust-a program to eliminate artifacts from next generation sequencing data. Bioinformatics 25: 2839-2840.
28. Kip1 tumor suppressor by miR-221 and miR-222 promotes cancer cell proliferation. EMBO J 26: 3699-3708.
29. Lehrbach NJ, Armisen J, Lightfoot HL, Murfitt KJ, Bugaut A, Balasubramanian S, Miska EA. 2009. LIN-28 and the poly(U) polymerase PUP-2 regulate let-7 microRNA processing in Caenorhabditis elegans. Nat Struct Mol Biol 16: 1016-1020.
30. Li J, Yang Z, Yu B, Liu J, Chen X. 2005. Methylation protects miRNAs and siRNAs from a 3′-end uridylation activity in Arabidopsis. Curr Biol 15: 1501-1507.
31. Liu J, Carmell MA, Rivas FV, Marsden CG, Thomson JM, Song JJ, Hammond SM, Joshua-Tor L, Hannon GJ. 2004. Argonaute2 is the catalytic engine of mammalian RNAi. Science 305: 1437-1441.
32. -ΔΔC(T) method. Methods 25: 402-408.
33. Lu S, Sun YH, Chiang VL. 2009. Adenylation of plant miRNAs. Nucleic Acids Res 37: 1878-1885.
34. Luzi E, Marini F, Sala SC, Tognarini I, Galli G, Brandi ML. 2008. Osteogenic differentiation of human adipose tissue-derived stem cells is modulated by the miR-26a targeting of the SMAD1 transcription factor. J Bone Miner Res 23: 287-295.
35. Marson A, Levine SS, Cole MF, Frampton GM, Brambrink T, Johnstone S, Guenther MG, Johnston WK, Wernig M, Newman J, et al. 2008. Connecting microRNA genes to the core transcriptional regulatory circuitry of embryonic stem cells. Cell 134: 521-533.
36. Martin G, Keller W. 2007. RNA-specific ribonucleotidyl transferases. RNA 13: 1834-1849.
37. Matranga C, Tomari Y, Shin C, Bartel DP, Zamore PD. 2005. Passenger-strand cleavage facilitates assembly of siRNA into Ago2-containing RNAi enzyme complexes. Cell 123: 607-620.
38. Mayr C, Bartel DP. 2009. Widespread shortening of 39 UTRs by alternative cleavage and polyadenylation activates oncogenes in cancer cells. Cell 138: 673-684.
39. Mayr C, Hemann MT, Bartel DP. 2007. Disrupting the pairing between let-7 and Hmga2 enhances oncogenic transformation. Science 315: 1576-1579. (Pubitemid 46449474)
40. Meister G, Landthaler M, Patkaniowska A, Dorsett Y, Teng G, Tuschl T. 2004. Human Argonaute2 mediates RNA cleavage targeted by miRNAs and siRNAs. Mol Cell 15: 185-197.
41. Mellman DL, Gonzales ML, Song C, Barlow CA, Wang P, Kendziorski C, Anderson RA. 2008. A PtdIns4,5P2-regulated nuclear poly(A) polymerase controls expression of select mRNAs. Nature 451: 1013-1017.
42. Muljo SA, Kanellopoulou C, Aravind L. 2009. MicroRNA targeting in mammalian genomes: Genes and mechanisms. Wiley Interdiscip Rev Syst Biol Med 2: 148-161.
43. Nakanishi T, Kubota H, Ishibashi N, Kumagai S, Watanabe H, Yamashita M, Kashiwabara S, Miyado K, Baba T. 2006. Possible role of mouse poly(A) polymerase mGLD-2 during oocyte maturation. Dev Biol 289: 115-126.
44. Petrocca F, Vecchione A, Croce CM. 2008a. Emerging role of miR-106b-25/ miR-17-92 clusters in the control of transforming growth factor beta signaling. Cancer Res 68: 8191-8194.
45. Petrocca F, Visone R, Onelli MR, Shah MH, Nicoloso MS, de Martino I, Iliopoulos D, Pilozzi E, Liu CG, Negrini M, et al. 2008b. E2F1-regulated microRNAs impair TGFbeta-dependent cell-cycle arrest and apoptosis in gastric cancer. Cancer Cell 13: 272-286.
46. Ramachandran V, Chen X. 2008. Degradation of microRNAs by a family of exoribonucleases in Arabidopsis. Science 321: 1490-1492.
47. Rand TA, Petersen S, Du F, Wang X. 2005. Argonaute2 cleaves the anti-guide strand of siRNA during RISC activation. Cell 123: 621-629.
48. Scott GK, Mattie MD, Berger CE, Benz SC, Benz CC. 2006. Rapid alteration of microRNA levels by histone deacetylase inhibition. Cancer Res 66: 1277-1281.
49. Severin J, Waterhouse AM, Kawaji H, Lassmann T, van Nimwegen E, Balwierz PJ, de Hoon ML, Hume DA, Carninci P, Hayashizaki Y, et al. 2009. FANTOM4 EdgeExpressDB: an integrated database of promoters, genes, microRNAs, expression dynamics and regulatory interactions. Genome Biol 10: r39. doi: 10.1186/gb-2009-10-4-r39.
50. Suh N, Jedamzik B, Eckmann CR, Wickens M, Kimble J. 2006. The GLD-2 poly(A) polymerase activates gld-1 mRNA in the Caenorhabditis elegans germ line. Proc Natl Acad Sci 103: 15108-15112.
51. Taft RJ, Glazov EA, Cloonan N, Simons C, Stephen S, Faulkner GJ, Lassmann T, Forrest AR, Grimmond SM, Schroder K, et al. 2009. Tiny RNAs associated with transcription start sites in animals. Nat Genet 41: 572-578.
52. Tomari Y, Du T, Zamore PD. 2007. Sorting of Drosophila small silencing RNAs. Cell 130: 299-308.
53. Tomaru Y, Nakanishi M, Miura H, Kimura Y, Ohkawa H, Ohta Y, Hayashizaki Y, Suzuki M. 2009. Identification of an inter-transcription factor regulatory network in human hepatoma cells by Matrix RNAi. Nucleic Acids Res 37: 1049-1060.
54. Trippe R, Sandrock B, Benecke BJ. 1998. A highly specific terminal uridylyl transferase modifies the 39-end of U6 small nuclear RNA. Nucleic Acids Res 26: 3119-3126.
55. Ventura A, Young AG, Winslow MM, Lintault L, Meissner A, Erkeland SJ, Newman J, Bronson RT, Crowley D, Stone JR, et al. 2008. Targeted deletion reveals essential and overlapping functions of the miR-17 through 92 family of miRNA clusters. Cell 132: 875-886.
56. Wang L, Eckmann CR, Kadyk LC, Wickens M, Kimble J. 2002. A regulatory cytoplasmic poly(A) polymerase in Caenorhabditis elegans. Nature 419: 312-316.
57. Xiao C, Srinivasan L, Calado DP, Patterson HC, Zhang B, Wang J, Henderson JM, Kutok JL, Rajewsky K. 2008. Lymphoproliferative disease and autoimmunity in mice with increased miR-17-92 expression in lymphocytes. Nat Immunol 9: 405-414. (Pubitemid 351405110)
58. Yoda M, Kawamata T, Paroo Z, Ye X, Iwasaki S, Liu Q, Tomari Y. 2010. ATP-dependent human RISC assembly pathways. Nat Struct Mol Biol 17: 17-23.