RNA decay via 3' uridylation

Biochimica et Biophysica Acta - Gene Regulatory Mechanisms

Volumn 1829, Issue 6-7, 2013, Pages 654-665

  Scott, Daniel D ^a   Norbury, Chris J ^a  

^a UNIVERSITY OF OXFORD   (United Kingdom)

Author keywords

Decapping; Lin28; MicroRNA; MRNA degradation; Piwi interacting RNA; TUTase

Indexed keywords

MESSENGER RNA; MICRORNA; PIWI INTERACTING RNA; RIBOSOME RNA; RNA;

3' URIDYLATION; CHEMICAL REACTION; HUMAN; NONHUMAN; NONSENSE MEDIATED MRNA DECAY; PRIORITY JOURNAL; REVIEW; RNA CLEAVAGE; RNA DEGRADATION; RNA STABILITY;

ANIMALS; CAENORHABDITIS ELEGANS; EUKARYOTA; HUMANS; MICRORNAS; NUCLEOTIDYLTRANSFERASES; PHYLOGENY; POLYNUCLEOTIDE ADENYLYLTRANSFERASE; RNA STABILITY; URIDINE; ZEBRAFISH;

EUKARYOTA;

EID: 84877823397     PISSN: 18749399     EISSN: 18764320     Source Type: Journal    
DOI: 10.1016/j.bbagrm.2013.01.009     Document Type: Review

References (168)

1. Rissland O.S., Norbury C.J. The Cid1 poly(U) polymerase. Biochim. Biophys. Acta, Gene Regul. Mech. 2008, 1779:286-294.
2. Souret F.F., Kastenmayer J.P., Green P.J. AtXRN4 degrades mRNA in Arabidopsis and its substrates include selected miRNA targets. Mol. Cell 2004, 15:173-183.
3. Shen B.Z., Goodman H.M. Uridine addition after microRNA-directed cleavage. Science 2004, 306:997.
4. Furnari F.B., Adams M.D., Pagano J.S. Unconventional processing of the 3' termini of the Epstein-Barr Virus DNA polymerase messenger RNA. PNAS 1993, 90:378-382.
5. Pfeffer S., Zavolan M., Grasser F.A., Chien M., Russo J.J., Ju J., John B., Enright A.J., Marks D., Sander C., Tuschl T. Identification of virus-encoded microRNAs. Science 2004, 304:734-736.
6. Ibrahim F., Rohr J., Jeong W.-J., Hesson J., Cerutti H. Untemplated oligoadenylation promotes degradation of RISC-cleaved transcripts. Science 2006, 314:1893.
7. Ibrahim F., Rymarquis L.A., Kim E.-J., Becker J., Balassa E., Green P.J., Cerutti H. Uridylation of mature miRNAs and siRNAs by the MUT68 nucleotidyltransferase promotes their degradation in Chlamydomonas. PNAS 2010, 107:3906-3911.
8. Chen C.Y., Shyu A.B. Mechanisms of deadenylation-dependent decay. WIREs: RNA 2011, 2:167-183.
9. Goldstrohm A.C., Wickens M. Multifunctional deadenylase complexes diversify mRNA control. Nat. Rev. Mol. Cell Biol. 2008, 9:337-344.
10. Wang S.W., Norbury C., Harris A.L., Toda T. Caffeine can override the S-M checkpoint in fission yeast. J. Cell Sci. 1999, 112:927-937.
11. Wang S.-W., Toda T., MacCallum R., Harris A.L., Norbury C. Cid1, a fission yeast protein required for S-M checkpoint control when DNA polymerase delta or epsilon is inactivated. Mol. Cell. Biol. 2000, 20:3234-3244.
12. Read R.L., Martinho R.G., Wang S.W., Carr A.M., Norbury C.J. Cytoplasmic poly(A) polymerases mediate cellular responses to S phase arrest. PNAS 2002, 99:12079-12084.
13. Rissland O.S., Mikulasova A., Norbury C.J. Efficient RNA polyuridylation by noncanonical poly(A) polymerases. Mol. Cell. Biol. 2007, 27:3612-3624.
14. Rissland O.S., Norbury C.J. Decapping is preceded by 3' uridylation in a novel pathway of bulk mRNA turnover. Nat. Struct. Mol. Biol. 2009, 16:616-624.
15. Song M.G., Kiledjian M. 3' terminal oligo U-tract-mediated stimulation of decapping. RNA 2007, 13:2356-2365.
16. Chowdhury A., Mukhopadhyay J., Tharun S. The decapping activator Lsm1p-7p-Pat1p complex has the intrinsic ability to distinguish between oligoadenylated and polyadenylated RNAs. RNA 2007, 13:998-1016.
17. Morozov I.Y., Jones M.G., Razak A.A., Rigden D.J., Caddick M.X. CUCU modification of mRNA promotes decapping and transcript degradation in Aspergillus nidulans. Mol. Cell. Biol. 2010, 30:460-469.
18. Morozov I.Y., Jones M.G., Spiller D.G., Rigden D.J., Dattenbock C., Novotny R., Strauss J., Caddick M.X. Distinct roles for Caf1, Ccr4, Edc3 and CutA in the co-ordination of transcript deadenylation, decapping and P-body formation in Aspergillus nidulans. Mol. Microbiol. 2010, 76:503-516.
19. Aravind L., Koonin E.V. DNA polymerase beta-like nucleotidyltransferase superfamily: identification of three new families, classification and evolutionary history. Nucleic Acids Res. 1999, 27:1609-1618.
20. Badis G., Saveanu C., Fromont-Racine M., Jacquier A. Targeted mRNA degradation by deadenylation-independent decapping. Mol. Cell 2004, 15:5-15.
21. Muhlrad D., Parker R. The yeast EDC1 mRNA undergoes deadenylation-independent decapping stimulated by Not2p, Not4p, and Not5p. EMBO J. 2005, 24:1033-1045.
22. Morrissey J.P., Deardorff J.A., Hebron C., Sachs A.B. Decapping of stabilized, polyadenylated mRNA in yeast pab1 mutants. Yeast 1999, 15:687-702.
23. Dominski Z., Marzluff W.F. Formation of the 3' end of histone mRNA. Gene 1999, 239:1-14.
24. Sullivan K.D., Mullen T.E., Marzluff W.F., Wagner E.J. Knockdown of SLBP results in nuclear retention of histone mRNA. RNA 2009, 15:459-472.
25. Sanchez R., Marzluff W.F. The stem-loop binding protein is required for efficient translation of histone mRNA in vivo and in vitro. Mol. Cell. Biol. 2002, 22:7093-7104.
26. Lyons T., Murray K.E., Roberts A.W., Barton D.J. Poliovirus 5'-terminal cloverleaf RNA is required in cis for VPg uridylylation and the initiation of negative-strand RNA synthesis. J. Virol. 2001, 75:10696-10708.
27. Meeks-Wagner D., Hartwell L.H. Normal stoichiometry of histone dimer sets is necessary for high fidelity of mitotic chromosome transmission. Cell 1986, 44:43-52.
28. Dominski Z., Yang X.C., Kaygun H., Dadlez M., Marzluff W.F. A 3' exonuclease that specifically interacts with the 3' end of histone mRNA. Mol. Cell 2003, 12:295-305.
29. Kennedy S., Wang D., Ruvkun G. A conserved siRNA-degrading RNase negatively regulates RNA interference in C. elegans. Nature 2004, 427:645-649.
30. Duchaine T.F., Wohlschlegel J.A., Kennedy S., Bei Y., Conte D., Pang K., Brownell D.R., Harding S., Mitani S., Ruvkun G., Yates J.R., Mello C.C. Functional proteomics reveals the biochemical niche of C. elegans DCR-1 in multiple small-RNA-mediated pathways. Cell 2006, 124:343-354.
31. Pavelec D.M., Lachowiec J., Duchaine T.F., Smith H.E., Kennedy S. Requirement for the ERI/DICER complex in endogenous RNA interference and sperm development in Caenorhabditis elegans. Genetics 2009, 183:1283-1295.
32. Ansel K.M., Pastor W.A., Rath N., Lapan A.D., Glasmacher E., Wolf C., Smith L.C., Papadopoulou N., Lamperti E.D., Tahiliani M., Ellwart J.W., Shi Y., Kremmer E., Rao A., Heissmeyer V. Mouse Eri1 interacts with the ribosome and catalyzes 5.8S rRNA processing. Nat. Struct. Mol. Biol. 2008, 15:523-530.
33. Gonzales M.L., Mellman D.L., Anderson R.A. CKIα is associated with and phosphorylates Star-PAP and is also required for expression of select Star-PAP target messenger RNAs. J. Biol. Chem. 2008, 283:12665-12673.
34. Tan D., Marzluff W.F., Dominski Z., Tong L. Structure of histone mRNA stem-loop, human stem-loop binding protein, and 3'hExo ternary complex. Science 2013, 339:318-321.
35. Hoefig K.P., Rath N., Heinz G.A., Wolf C., Dameris J., Schepers A., Kremmer E., Ansel K.M., Heissmeyer V. Eri1 degrades the stem-loop of oligouridylated histone mRNAs to induce replication-dependent decay. Nat. Struct. Mol. Biol. 2013, 20:73-81.
36. Kaygun H., Marzluff W.F. Regulated degradation of replication-dependent histone mRNAs requires both ATR and Upf1. Nat. Struct. Mol. Biol. 2005, 12:794-800.
37. Müller B., Blackburn J., Feijoo C., Zhao X., Smythe C. DNA-activated protein kinase functions in a newly observed S phase checkpoint that links histone mRNA abundance with DNA replication. J. Cell Biol. 2007, 179:1385-1398.
38. Graves R.A., Pandey N.B., Chodchoy N., Marzluff W.F. Translation is required for regulation of histone mRNA degradation. Cell 1987, 48:615-626.
39. Ross J., Peltz S.W., Kobs G., Brewer G. Histone mRNA degradation in vivo: the first detectable step occurs at or near the 3' terminus. Mol. Cell. Biol. 1986, 6:4362-4371.
40. Mullen T.E., Marzluff W.F. Degradation of histone mRNA requires oligouridylation followed by decapping and simultaneous degradation of the mRNA both 5' to 3' and 3' to 5'. Genes Dev. 2008, 22:50-65.
41. Su W., Slepenkov S.V., Slevin M.K., Lyons S.M., Ziemniak M., Kowalska J., Darzynkiewicz E., Jemielity J., Marzluff W.F., Rhoads R.E. mRNAs containing the histone 3' stem-loop are degraded primarily by decapping mediated by oligouridylation of the 3' end. RNA 2013, 19:1-16.
42. Schmidt M.J., West S., Norbury C.J. The human cytoplasmic RNA terminal U-transferase ZCCHC11 targets histone mRNAs for degradation. RNA 2011, 17:39-44.
43. Nagaike T., Suzuki T., Katoh T., Ueda T. Human mitochondrial mRNAs are stabilized with polyadenylation regulated by mitochondria-specific poly(A) polymerase and polynucleotide phosphorylase. J. Biol. Chem. 2005, 280:19721-19727.
44. Tomecki R., Dmochowska A., Gewartowski K., Dziembowski A., Stepien P.P. Identification of a novel human nuclear-encoded mitochondrial poly(A) polymerase. Nucleic Acids Res. 2004, 32:6001-6014.
45. Shcherbik N., Wang M., Lapik Y.R., Srivastava L., Pestov D.G. Polyadenylation and degradation of incomplete RNA polymerase I transcripts in mammalian cells. EMBO Rep. 2010, 11:106-111.
46. Ambros V., Horvitz H.R. Heterochronic mutants of the nematode Caenorhabditis elegans. Science 1984, 226:409-416.
47. Thornton J.E., Gregory R.I. How does Lin28 let-7 control development and disease?. Trends Cell Biol. 2012, 22:1-9.
48. Yu J.Y., Vodyanik M.A., Smuga-Otto K., Antosiewicz-Bourget J., Frane J.L., Tian S., Nie J., Jonsdottir G.A., Ruotti V., Stewart R., Slukvin I.I., Thomson J.A. Induced pluripotent stem cell lines derived from human somatic cells. Science 2007, 318:1917-1920.
49. Büssing I., Slack F.J., Grosshans H. let-7 microRNAs in development, stem cells and cancer. Trends Mol. Med. 2008, 14:400-409.
50. Van Wynsberghe P.M., Kai Z.S., Massirer K.B., Burton V.H., Yeo G.W., Pasquinelli A.E. LIN-28 co-transcriptionally binds primary let-7 to regulate miRNA maturation in Caenorhabditis elegans. Nat. Struct. Mol. Biol. 2011, 18:302-308.
51. Newman M.A., Thomson J.M., Hammond S.M. Lin-28 interaction with the Let-7 precursor loop mediates regulated microRNA processing. RNA 2008, 14:1539-1549.
52. Viswanathan S.R., Daley G.Q., Gregory R.I. Selective blockade of microRNA processing by Lin28. Science 2008, 320:97-100.
53. Heo I., Joo C., Cho J., Ha M., Han J., Kim V.N. Lin28 mediates the terminal uridylation of let-7 precursor microRNA. Mol. Cell 2008, 32:276-284.
54. Lightfoot H.L., Bugaut A., Armisen J., Lehrbach N.J., Miska E.A., Balasubramanian S. A LIN28-dependent structural change in pre-let-7g directly inhibits Dicer processing. Biochemistry 2011, 50:7514-7521.
55. Rybak A., Fuchs H., Smirnova L., Brandt C., Pohl E.E., Nitsch R., Wulczyn F.G. A feedback loop comprising lin-28 and let-7 controls pre-let-7 maturation during neural stem-cell commitment. Nat. Cell Biol. 2008, 10:987-993.
56. Piskounova E., Polytarchou C., Thornton Jamesâ E., LaPierre Robertâ J., Pothoulakis C., Hagan Johnâ P., Iliopoulos D., Gregory Richardâ I. Lin28A and Lin28B inhibit let-7 microRNA biogenesis by distinct mechanisms. Cell 2011, 147:1066-1079.
57. Jones M.R., Quinton L.J., Blahna M.T., Neilson J.R., Fu S.N., Ivanov A.R., Wolf D.A., Mizgerd J.P. Zcchc11-dependent uridylation of microRNA directs cytokine expression. Nat. Cell Biol. 2009, 11:1157-U1258.
58. Yeom K.-H., Heo I., Lee J., Hohng S., Kim V.N., Joo C. Single-molecule approach to immunoprecipitated protein complexes: insights into miRNA uridylation. EMBO Rep. 2011, 12:690-696.
59. Heo I., Joo C., Kim Y.K., Ha M., Yoon M.J., Cho J., Yeom K.H., Han J., Kim V.N. TUT4 in concert with Lin28 suppresses microRNA biogenesis through pre-microRNA uridylation. Cell 2009, 138:696-708.
60. Thornton J.E., Chang H.-M., Piskounova E., Gregory R.I. Lin28-mediated control of let-7 microRNA expression by alternative TUTases Zcchc11 (TUT4) and Zcchc6 (TUT7). RNA 2012, 18:1875-1885.
61. Hagan J.P., Piskounova E., Gregory R.I. Lin28 recruits the TUTase Zcchc11 to inhibit let-7 maturation in mouse embryonic stem cells. Nat. Struct. Mol. Biol. 2009, 16:1021-U1033.
62. Mayr F., Schütz A., Döge N., Heinemann U. The Lin28 cold-shock domain remodels pre-let-7 microRNA. Nucleic Acids Res. 2012, 40:7492-7506.
63. Nam Y., Chen C., Gregory Richard I., Chou James J., Sliz P. Molecular basis for interaction of let-7 MicroRNAs with Lin28. Cell 2011, 147:1080-1091.
64. Desjardins A., Yang A., Bouvette J., Omichinski J.G., Legault P. Importance of the NCp7-like domain in the recognition of pre-let-7g by the pluripotency factor Lin28. Nucleic Acids Res. 2012, 40:1767-1777.
65. Lehrbach N.J., Armisen J., Lightfoot H.L., Murfitt K.J., Bugaut A., Balasubramanian S., Miska E.A. LIN-28 and the poly(U) polymerase PUP-2 regulate let-7 microRNA processing in Caenorhabditis elegans. Nat. Struct. Mol. Biol. 2009, 16:1016-U1027.
66. Kwak J.E., Wickens M. A family of poly(U) polymerases. RNA 2007, 13:860-867.
67. Heo I., Ha M., Lim J., Yoon M.J., Park J.E., Kwon S.C., Chang H., Kim V.N. Mono-uridylation of pre-microRNA as a key step in the biogenesis of group II let-7 microRNAs. Cell 2012, 151:521-532.
68. Newman M.A., Mani V., Hammond S.M. Deep sequencing of microRNA precursors reveals extensive 3' end modification. RNA 2011, 17:1795-1803.
69. Chen X., Liu J., Cheng Y., Jia D. HEN1 functions pleiotropically in Arabidopsis development and acts in C function in the flower. Development 2002, 129:1085-1094.
70. Park W., Li J., Song R., Messing J., Chen X. CARPEL FACTORY, a Dicer Homolog, and HEN1, a novel protein, act in microRNA metabolism in Arabidopsis thaliana. Curr. Biol. 2002, 12:1484-1495.
71. Boutet S., Vazquez F., Liu J., Béclin C., Fagard M., Gratias A., Morel J.-B., Crété P., Chen X., Vaucheret H. Arabidopsis HEN1: a genetic link between endogenous miRNA controlling development and siRNA controlling transgene silencing and virus resistance. Curr. Biol. 2003, 13:843-848.
72. Yu B., Yang Z., Li J., Minakhina S., Yang M., Padgett R.W., Steward R., Chen X. Methylation as a crucial step in plant microRNA biogenesis. Science 2005, 307:932-935.
73. Li J.J., Yang Z.Y., Yu B., Liu J., Chen X.M. Methylation protects miRNAs and siRNAs from a 3'-end uridylation activity in Arabidopsis. Curr. Biol. 2005, 15:1501-1507.
74. Yang Z., Ebright Y.W., Yu B., Chen X. HEN1 recognizes 21-24 nt small RNA duplexes and deposits a methyl group onto the 2' OH of the 3' terminal nucleotide. Nucleic Acids Res. 2006, 34:667-675.
75. Ren G., Chen X., Yu B. Uridylation of miRNAs by hen1 suppressor1 in Arabidopsis. Curr. Biol. 2012, 22:695-700.
76. Zhao Y., Yu Y., Zhai J., Ramachandran V., Dinh T.T., Meyers B.C., Mo B., Chen X. The Arabidopsis nucleotidyl transferase HESO1 uridylates unmethylated small RNAs to trigger their degradation. Curr. Biol. 2012, 22:689-694.
77. Yu B., Chapman E.J., Yang Z., Carrington J.C., Chen X. Transgenically expressed viral RNA silencing suppressors interfere with microRNA methylation in Arabidopsis. FEBS Lett. 2006, 580:3117-3120.
78. Akbergenov R., Si-Ammour A., Blevins T., Amin I., Kutter C., Vanderschuren H., Zhang P., Gruissem W., Meins F., Hohn T., Pooggin M.M. Molecular characterization of geminivirus-derived small RNAs in different plant species. Nucleic Acids Res. 2006, 34:462-471.
79. Billi A.C., Alessi A.F., Khivansara V., Han T., Freeberg M., Mitani S., Kim J.K. The Caenorhabditis elegans HEN1 ortholog, HENN-1, methylates and stabilizes select subclasses of germline small RNAs. PLoS Genet. 2012, 8:e1002617.
80. Kamminga L.M., van Wolfswinkel J.C., Luteijn M.J., Kaaij L.J., Bagijn M.P., Sapetschnig A., Miska E.A., Berezikov E., Ketting R.F. Differential impact of the HEN1 homolog HENN-1 on 21U and 26G RNAs in the germline of Caenorhabditis elegans. PLoS Genet. 2012, 8:e1002702.
81. Montgomery T.A., Rim Y.-S., Zhang C., Dowen R.H., Phillips C.M., Fischer S.E.J., Ruvkun G. PIWI associated siRNAs and piRNAs specifically require the Caenorhabditis elegans HEN1 ortholog henn-1. PLoS Genet. 2012, 8:e1002616.
82. Ruby J.G., Jan C., Player C., Axtell M.J., Lee W., Nusbaum C., Ge H., Bartel D.P. Large-scale sequencing reveals 21U-RNAs and additional microRNAs and endogenous siRNAs in C. elegans. Cell 2006, 127:1193-1207.
83. Pélisson A., Sarot E., Payen-Groschêne G., Bucheton A. A novel repeat-associated small interfering RNA-mediated silencing pathway downregulates complementary sense gypsy transcripts in somatic cells f the Drosophila ovary. J. Virol. 2007, 81:1951-1960.
84. Vagin V.V., Sigova A., Li C., Seitz H., Gvozdev V., Zamore P.D. A distinct small RNA pathway silences selfish genetic elements in the germline. Science 2006, 313:320-324.
85. Horwich M.D., Li C., Matranga C., Vagin V., Farley G., Wang P., Zamore P.D. The Drosophila RNA methyltransferase, DmHen1, modifies germline piRNAs and single-stranded siRNAs in RISC. Curr. Biol. 2007, 17:1265-1272.
86. Saito K., Sakaguchi Y., Suzuki T., Suzuki T., Siomi H., Siomi M.C. Pimet, the Drosophila homolog of HEN1, mediates 2'-O-methylation of Piwi-interacting RNAs at their 3' ends. Genes Dev. 2007, 21:1603-1608.
87. Ameres S.L., Horwich M.D., Hung J.-H., Xu J., Ghildiyal M., Weng Z., Zamore P.D. Target RNA-directed trimming and tailing of small silencing RNAs. Science 2010, 328:1534-1539.
88. Ameres S.L., Hung J.-H., Xu J., Weng Z., Zamore P.D. Target RNA-directed tailing and trimming purifies the sorting of endo-siRNAs between the two Drosophila Argonaute proteins. RNA 2011, 17:54-63.
89. Kamminga L.M., Luteijn M.J., den Broeder M.J., Redl S., Kaaij L.J.T., Roovers E.F., Ladurner P., Berezikov E., Ketting R.F. Hen1 is required for oocyte development and piRNA stability in zebrafish. EMBO J. 2010, 29:3688-3700.
90. Houwing S., Kamminga L.M., Berezikov E., Cronembold D., Girard A., van den Elst H., Filippov D.V., Blaser H., Raz E., Moens C.B., Plasterk R.H., Hannon G.J., Draper B.W., Ketting R.F. A role for Piwi and piRNAs in germ cell maintenance and transposon silencing in Zebrafish. Cell 2007, 129:69-82.
91. Houwing S., Berezikov E., Ketting R.F. Zili is required for germ cell differentiation and meiosis in zebrafish. EMBO J. 2008, 27:2702-2711.
92. Molnár A., Schwach F., Studholme D.J., Thuenemann E.C., Baulcombe D.C. miRNAs control gene expression in the single-cell alga Chlamydomonas reinhardtii. Nature 2007, 447:1126-1129.
93. LaCava J., Houseley J., Saveanu C., Petfalski E., Thompson E., Jacquier A., Tollervey D. RNA degradation by the exosome is promoted by a nuclear polyadenylation complex. Cell 2005, 121:713-724.
94. Vaňáčová S., Wolf J., Martin G., Blank D., Dettwiler S., Friedlein A., Langen H., Keith G., Keller W. A new yeast poly(A) polymerase complex involved in RNA quality control. PLoS Biol. 2005, 3:986-997.
95. Wyers F., Rougemaille M., Badis G., Rousselle J.C., Dufour M.E., Boulay J., Regnault B., Devaux F., Namane A., Seraphin B., Libri D., Jacquier A. Cryptic Pol II transcripts are degraded by a nuclear quality control pathway involving a new poly(A) polymerase. Cell 2005, 121:725-737.
96. Kirino Y., Mourelatos Z. Mouse Piwi-interacting RNAs are 2'-O-methylated at their 3' termini. Nat. Struct. Mol. Biol. 2007, 14:347-348.
97. Ohara T., Sakaguchi Y., Suzuki T., Ueda H., Miyauchi K., Suzuki T. The 3' termini of mouse Piwi-interacting RNAs are 2'-O-methylated. Nat. Struct. Mol. Biol. 2007, 14:349-350.
98. Kirino Y., Mourelatos Z. The mouse homolog of HEN1 is a potential methylase for Piwi-interacting RNAs. RNA 2007, 13:1397-1401.
99. Kurth H.M., Mochizuki K. 2'-O-methylation stabilizes Piwi-associated small RNAs and ensures DNA elimination in Tetrahymena. RNA 2009, 15:675-685.
100. Kawaoka S., Izumi N., Katsuma S., Tomari Y. 3' end formation of PIWI-interacting RNAs in vitro. Mol. Cell 2011, 43:1015-1022.
101. Huang Y., Ji L., Huang Q., Vassylyev D.G., Chen X., Ma J.B. Structural insights into mechanisms of the small RNA methyltransferase HEN1. Nature 2009, 461:823-827.
102. Tkaczuk K.L., Obarska A., Bujnicki J.M. Molecular phylogenetics and comparative modeling of HEN1, a methyltransferase involved in plant microRNA biogenesis. BMC Evol. Biol. 2006, 6:6.
103. Klattenhoff C., Theurkauf W. Biogenesis and germline functions of piRNAs. Development 2008, 135:3-9.
104. Sashital D.G., Doudna J.A. Structural insights into RNA interference. Curr. Opin. Struct. Biol. 2010, 20:90-97.
105. Claycomb J.M., Batista P.J., Pang K.M., Gu W.F., Vasale J.J., van Wolfswinkel J.C., Chaves D.A., Shirayama M., Mitani S., Ketting R.F., Conte D., Mello C.C. The Argonaute CSR-1 and Its 22G-RNA cofactors are required for holocentric chromosome segregation. Cell 2009, 139:123-134.
106. Aravin A.A., van der Heijden G.W., Castaneda J., Vagin V.V., Hannon G.J., Bortvin A. Cytoplasmic compartmentalization of the fetal piRNA pathway in mice. PLoS Genet. 2009, 5:e1000764.
107. Batista P.J., Ruby J.G., Claycomb J.M., Chiang R., Fahlgren N., Kasschau K.D., Chaves D.A., Gu W., Vasale J.J., Duan S., Conte D., Luo S., Schroth G.P., Carrington J.C., Bartel D.P., Mello C.C. PRG-1 and 21U-RNAs interact to form the piRNA complex required for fertility in C. elegans. Mol. Cell 2008, 31:67-78.
108. Wang G., Reinke V. A C. elegans Piwi, PRG-1, regulates 21U-RNAs during spermatogenesis. Curr. Biol. 2008, 18:861-867.
109. Gu W., Shirayama M., Conte D., Vasale J., Batista P.J., Claycomb J.M., Moresco J.J., Youngman E.M., Keys J., Stoltz M.J., Chen C.-C.G., Chaves D.A., Duan S., Kasschau K.D., Fahlgren N., Yates Iii J.R., Mitani S., Carrington J.C., Mello C.C. Distinct Argonaute-mediated 22G-RNA pathways direct genome surveillance in the C. elegans germline. Mol. Cell 2009, 36:231-244.
110. Lingel A., Simon B., Izaurralde E., Sattler M. Nucleic acid 3'-end recognition by the Argonaute2 PAZ domain. Nat. Struct. Mol. Biol. 2004, 11:576-577.
111. Ma J.-B., Ye K., Patel D.J. Structural basis for overhang-specific small interfering RNA recognition by the PAZ domain. Nature 2004, 429:318-322.
112. Simon B., Kirkpatrick J.P., Eckhardt S., Reuter M., Rocha E.A., Andrade-Navarro M.A., Sehr P., Pillai R.S., Carlomagno T. Recognition of 2'-O-methylated 3'-end of piRNA by the PAZ domain of a Piwi protein. Structure 1993, 19(2011):172-180.
113. Tian Y., Simanshu D.K., Ma J.B., Patel D.J. Structural basis for piRNA 2'-O-methylated 3'-end recognition by Piwi PAZ (Piwi/Argonaute/Zwille) domains. PNAS 2011, 108:903-910.
114. Baccarini A., Chauhan H., Gardner T.J., Jayaprakash A.D., Sachidanandam R., Brown B.D. Kinetic analysis reveals the fate of a microRNA following target regulation in mammalian cells. Curr. Biol. 2011, 21:369-376.
115. van Wolfswinkel J.C., Claycomb J.M., Batista P.J., Mello C.C., Berezikov E., Ketting R.F. CDE-1 affects chromosome segregation through uridylation of CSR-1-bound siRNAs. Cell 2009, 139:135-148.
116. Robert V.J.P., Sijen T., van Wolfswinkel J., Plasterk R.H.A. Chromatin and RNAi factors protect the C. elegans germline against repetitive sequences. Genes Dev. 2005, 19:782-787.
117. Olsen A., Vantipalli M.C., Lithgow G.J. Checkpoint proteins control survival of the postmitotic cells in Caenorhabditis elegans. Science 2006, 312:1381-1385.
118. Win T.Z., Stevenson A.L., Wang S.W. Fission yeast Cid12 has dual functions in chromosome segregation and checkpoint control. Mol. Cell. Biol. 2006, 26:4435-4447.
119. Motamedi M.R., Verdel A., Colmenares S.U., Gerber S.A., Gygi S.P., Moazed D. Two RNAi complexes, RITS and RDRC, physically interact and localize to noncoding centromeric RNAs. Cell 2004, 119:789-802.
120. Win T.Z., Draper S., Read R.L., Pearce J., Norbury C.J., Wang S.W. Requirement of fission yeast Cid14 in polyadenylation of rRNAs. Mol. Cell. Biol. 2006, 26:1710-1721.
121. Chen C.-C.G., Simard M.J., Tabara H., Brownell D.R., McCollough J.A., Mello C.C. A Member of the polymerase β nucleotidyltransferase superfamily is required for RNA interference in C. elegans. Curr. Biol. 2005, 15:378-383.
122. Tabara H., Sarkissian M., Kelly W.G., Fleenor J., Grishok A., Timmons L., Fire A., Mello C.C. The rde-1 gene, RNA interference, and transposon silencing in C. elegans. Cell 1999, 99:123-132.
123. Katoh T., Sakaguchi Y., Miyauchi K., Suzuki T., Kashiwabara S.-i., Baba T., Suzuki T. Selective stabilization of mammalian microRNAs by 3' adenylation mediated by the cytoplasmic poly(A) polymerase GLD-2. Genes Dev. 2009, 23:433-438.
124. Wyman S.K., Knouf E.C., Parkin R.K., Fritz B.R., Lin D.W., Dennis L.M., Krouse M.A., Webster P.J., Tewari M. Post-transcriptional generation of miRNA variants by multiple nucleotidyl transferases contributes to miRNA transcriptome complexity. Genome Res. 2011, 21:1450-1461.
125. Landgraf P., Rusu M., Sheridan R., Sewer A., Iovino N., Aravin A., Pfeffer S., Rice A., Kamphorst A.O., Landthaler M., Lin C., Socci N.D., Hermida L., Fulci V., Chiaretti S., Foa R., Schliwka J., Fuchs U., Novosel A., Muller R.U., Schermer B., Bissels U., Inman J., Phan Q., Chien M., Weir D.B., Choksi R., De Vita G., Frezzetti D., Trompeter H.I., Hornung V., Teng G., Hartmann G., Palkovits M., Di Lauro R., Wernet P., Macino G., Rogler C.E., Nagle J.W., Ju J., Papavasiliou F.N., Benzing T., Lichter P., Tam W., Brownstein M.J., Bosio A., Borkhardt A., Russo J.J., Sander C., Zavolan M., Tuschl T. A mammalian microRNA expression atlas based on small RNA library sequencing. Cell 2007, 129:1401-1414.
126. Morin R.D., O'Connor M.D., Griffith M., Kuchenbauer F., Delaney A., Prabhu A.L., Zhao Y., McDonald H., Zeng T., Hirst M., Eaves C.J., Marra M.A. Application of massively parallel sequencing to microRNA profiling and discovery in human embryonic stem cells. Genome Res. 2008, 18:610-621.
127. Seitz H., Ghildiyal M., Zamore P.D. Argonaute loading improves the 5' precision of both microRNAs and their miRNA* strands in flies. Curr. Biol. 2008, 18:147-151.
128. Minoda Y., Saeki K., Aki D., Takaki H., Sanada T., Koga K., Kobayashi T., Takaesu G., Yoshimura A. A novel zinc finger protein, ZCCHC11, interacts with TIFA and modulates TLR signaling. Biochem. Biophys. Res. Commun. 2006, 344:1023-1030.
129. Wu H., Neilson J.R., Kumar P., Manocha M., Shankar P., Sharp P.A., Manjunath N. miRNA profiling of naive, effector and memory CD8 T cells. PLoS One 2007, 2:e1020.
130. Chiang H.R., Schoenfeld L.W., Ruby J.G., Auyeung V.C., Spies N., Baek D., Johnston W.K., Russ C., Luo S., Babiarz J.E., Blelloch R., Schroth G.P., Nusbaum C., Bartel D.P. Mammalian microRNAs: experimental evaluation of novel and previously annotated genes. Genes Dev. 2010, 24:992-1009.
131. Yates L.A., Fleurdépine S., Rissland O.S., De Colibus L., Harlos K., Norbury C.J., Gilbert R.J.C. Structural basis for the activity of a cytoplasmic RNA terminal uridylyl transferase. Nat. Struct. Mol. Biol. 2012, 19:782-787.
132. Han B.W., Hung J.H., Weng Z., Zamore P.D., Ameres S.L. The 3'-to-5' exoribonuclease Nibbler shapes the 3' ends of microRNAs bound to Drosophila Argonaute1. Curr. Biol. 2011, 21:1878-1887.
133. Liu N., Abe M., Sabin L.R., Hendriks G.J., Naqvi A.S., Yu Z., Cherry S., Bonini N.M. The exoribonuclease Nibbler controls 3' end processing of microRNAs in Drosophila. Curr. Biol. 2011, 21:1888-1893.
134. Xue Z., Yuan H., Guo J., Liu Y. Reconstitution of an Argonaute-dependent small RNA biogenesis pathway reveals a handover mechanism involving the RNA exosome and the exonuclease QIP. Mol. Cell 2012, 46:299-310.
135. Iida T., Kawaguchi R., Nakayama J.-i. Conserved ribonuclease, Eri1, negatively regulates heterochromatin assembly in fission yeast. Curr. Biol. 2006, 16:1459-1464.
136. Ramachandran V., Chen X. Degradation of microRNAs by a family of exoribonucleases in Arabidopsis. Science 2008, 321:1490-1492.
137. Mellman D.L., Anderson R.A. A novel gene expression pathway regulated by nuclear phosphoinositides. Advances in Enzyme Regulation 2009, vol. 49:11-28. G. Weber, C.E. Forrest Weber, L. Cocco (Eds.).
138. Mellman D.L., Gonzales M.L., Song C.H., Barlow C.A., Wang P., Kendziorski C., Anderson R.A. A PtdIns4,5P(2)-regulated nuclear poly(A) polymerase controls expression of select mRNAs. Nature 2008, 451:1013-1017.
139. Trippe R., Guschina E., Hossbach M., Urlaub H., Lührmann R., Benecke B.-J. Identification, cloning, and functional analysis of the human U6 snRNA-specific terminal uridylyl transferase. RNA 2006, 12:1494-1504.
140. Trippe R., Richly H., Benecke B.-J. Biochemical characterization of a U6 small nuclear RNA-specific terminal uridylyltransferase. Eur. J. Biochem. 2003, 270:971-980.
141. Kwak J.E., Wang L.T., Ballantyne S., Kimble J., Wickens M. Mammalian GLD-2 homologs are poly(A) polymerases. PNAS 2004, 101:4407-4412.
142. Rouhana L., Wang L., Buter N., Kwak J.E., Schiltz C.A., Gonzalez T., Kelley A.E., Landry C.F., Wickens M. Vertebrate GLD2 poly(A) polymerases in the germline and the brain. RNA 2005, 11:1117-1130.
143. Glahder J.A., Norrild B. Involvement of hGLD-2 in cytoplasmic polyadenylation of human p53 mRNA. Acta Pathol. Microbiol. Immunol. Scand. 2011, 119:769-775.
144. Barnard D.C., Ryan K., Manley J.L., Richter J.D. Symplekin and xGLD-2 are required for CPEB-mediated cytoplasmic polyadenylation. Cell 2004, 119:641-651.
145. Kim J.H., Richter J.D. Opposing polymerase-deadenylase activities regulate cytoplasmic polyadenylation. Mol. Cell 2006, 24:173-183.
146. Radford H.E., Meijer H.A., de Moor C.H. Translational control by cytoplasmic polyadenylation in Xenopus oocytes. Biochim. Biophys. Acta, Gene Regul. Mech. 2008, 1779:217-229.
147. Berndt H., Harnisch C., Rammelt C., Stohr N., Zirkel A., Dohm J.C., Himmelbauer H., Tavanez J.P., Huttelmaier S., Wahle E. Maturation of mammalian H/ACA box snoRNAs: PAPD5-dependent adenylation and PARN-dependent trimming. RNA 2012, 18:958-972.
148. Rammelt C., Bilen B., Zavolan M., Keller W. PAPD5, a noncanonical poly(A) polymerase with an unusual RNA-binding motif. RNA 2011, 17:1737-1746.
149. Nakamura R., Takeuchi R., Takata K., Shimanouchi K., Abe Y., Kanai Y., Ruike T., Ihara A., Sakaguchi K. TRF4 is involved in polyadenylation of snRNAs in Drosophila melanogaster. Mol. Cell. Biol. 2008, 28:6620-6631.
150. Kwak J.E., Drier E., Barbee S.A., Ramaswami M., Yin J.C.P., Wickens M. GLD2 poly(A) polymerase is required for long-term memory. PNAS 2008, 105:14644-14649.
151. Benoit P., Papin C., Kwak J.E., Wickens M., Simonelig M. PAP- and GLD-2-type poly(A) polymerases are required sequentially in cytoplasmic polyadenylation and oogenesis in Drosophila. Development 2008, 135:1969-1979.
152. Schmid M., Kuchler B., Eckmann C.R. Two conserved regulatory cytoplasmic poly(A) polymerases, GLD-4 and GLD-2, regulate meiotic progression in C. elegans. Genes Dev. 2009, 23:824-836.
153. Kim K.W., Wilson T.L., Kimble J. GLD-2/RNP-8 cytoplasmic poly(A) polymerase is a broad-spectrum regulator of the oogenesis program. PNAS 2010, 107:17445-17450.
154. Suh N., Jedamzik B., Eckmann C.R., Wickens M., Kimble J. The GLD-2 poly(A) polymerase activates gld-1 mRNA in the Caenorhabditis elegans germ line. PNAS 2006, 103:15108-15112.
155. Wang L.T., Eckmann C.R., Kadyk L.C., Wickens M., Kimble J. A regulatory cytoplasmic poly(A) polymerase in Caenorhabditis elegans. Nature 2002, 419:312-316.
156. Saitoh S., Chabes A., McDonald W.H., Thelander L., Yates J.R., Russell P. Cid13 is a cytoplasmic poly(A) polymerase that regulates ribonucleotide reductase mRNA. Cell 2002, 109:563-573.
157. Buhler M., Haas W., Gygi S.P., Moazed D. RNAi-dependent and -independent RNA turnover mechanisms contribute to heterochromatic gene silencing. Cell 2007, 129:707-721.
158. Buhler M., Spies N., Bartel D.P., Moazed D. TRAMP-mediated RNA surveillance prevents spurious entry of RNAs into the Schizosaccharomyces pombe siRNA pathway. Nat. Struct. Mol. Biol. 2008, 15:1015-1023.
159. Lemieux C., Marguerat S., Lafontaine J., Barbezier N., Bahler J., Bachand F. A Pre-mRNA degradation pathway that selectively targets intron-containing genes requires the nuclear poly(A)-binding protein. Mol. Cell 2011, 44:108-119.
160. Wang S.W., Stevenson A.L., Kearsey S.E., Watt S., Bahler J. Global role for polyadenylation-assisted nuclear RNA degradation in posttranscriptional gene silencing. Mol. Cell. Biol. 2008, 28:656-665.
161. Houseley J., Kotovic K., El Hage A., Tollervey D. Trf4 targets ncRNAs from telomeric and rDNA spacer regions and functions in rDNA copy number control. EMBO J. 2007, 26:4996-5006.
162. Kadaba S., Wang X.Y., Anderson J.T. Nuclear RNA surveillance in Saccharomyces cerevisiae: Trf4p-dependent polyadenylation of nascent hypomethylated tRNA and an aberrant form of 5S rRNA. RNA 2004, 12:508-521.
163. Dickinson H., Tretbar S., Betat H., Morl M. The TRAMP complex shows tRNA editing activity in S. cerevisiae. Mol. Biol. Evol. 2012, 29:1451-1459.
164. Grzechnik P., Kufel J. Polyadenylation linked to transcription termination directs the processing of snoRNA precursors in yeast. Mol. Cell 2008, 32:247-258.
165. Roth K.M., Byam J., Fang F., Butler J.S. Regulation of NAB2 mRNA 3'-end formation requires the core exosome and the Trf4p component of the TRAMP complex. RNA 2009, 15:1045-1058.
166. San Paolo S., Vaňáčová S., Schenk L., Scherrer T., Blank D., Keller W., Gerber A.P. Distinct roles of non-canonical poly(A) polymerases in RNA metabolism. PLoS Genet. 2009, 5:e1000555.
167. Wery M., Ruidant S., Schillewaert S., Lepore N., Lafontaine D.L.J. The nuclear poly(A) polymerase and exosome cofactor Trf5 is recruited cotranscriptionally to nucleolar surveillance. RNA 2009, 15:406-419.
168. Houseley J., Tollervey D. Yeast Trf5p is a nuclear poly(A) polymerase. EMBO Rep. 2006, 7:205-211.