Uridylation prevents 3′ trimming of oligoadenylated mRNAs

Nucleic Acids Research

Volumn 41, Issue 14, 2013, Pages 7115-7127

  Sement, François Michaël ^a   Ferrier, Emilie ^a   Zuber, Hélène ^a   Merret, Rémy ^b   Alioua, Malek ^a   Deragon, Jean Marc ^b   Bousquet Antonelli, Cécile ^b   Lange, Heike ^a   Gagliardi, Dominique ^a  

^a UNIVERSITÉ DE STRASBOURG   (France)

^b CNRS   (France)

Author keywords

[No Author keywords available]

Indexed keywords

2',5' OLIGOADENYLIC ACID; HEXOSE 1 PHOSPHATE URIDYLYLTRANSFERASE; MESSENGER RNA; UNCLASSIFIED DRUG; URIDINE TRIPHOSPHATE; URIDINE TRIPHOSPHATE RNA URIDYLYLTRANSFERASE 1;

ADENYLATION; ARABIDOPSIS THALIANA; ARTICLE; BIOTRANSFORMATION; CONTROLLED STUDY; OLIGOADENYLATION; POLYSOME; PRIORITY JOURNAL; RNA DEGRADATION; URIDYLATION;

ADENINE NUCLEOTIDES; ARABIDOPSIS; ARABIDOPSIS PROTEINS; MUTATION; OLIGORIBONUCLEOTIDES; POLYRIBOSOMES; RNA 3' END PROCESSING; RNA NUCLEOTIDYLTRANSFERASES; RNA STABILITY; RNA, MESSENGER; URIDINE; URIDINE MONOPHOSPHATE;

EID: 84881494757     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gkt465     Document Type: Article

References (61)

1. Trippe R., Sandrock B. and Benecke B.J. (1998) A highly specific terminal uridylyl transferase modifies the 30-end of U6 small nuclear RNA. Nucleic Acids Res., 26, 3119-3126
2. Wilusz C.J. and Wilusz J. (2008) New ways to meet your (30) end oligouridylation as a step on the path to destruction. Genes Dev., 22, 1-7
3. Marzluff W. (2009) A new way to initiate mRNA degradation. Nat. Struct. Mol. Biol., 16, 613-614
4. Norbury C.J. (2010) 30 Uridylation and the regulation of RNA function in the cytoplasm. Biochem. Soc. Trans., 38, 1150-1153
5. Morozov I.Y. and Caddick M.X. (2012) Cytoplasmic mRNA 30 tagging in eukaryotes: Does it spell the end? Biochem. Soc. Trans., 40, 810-814
6. Heo I., Ha M., Lim J., Yoon M.J., Park J.E., Kwon S.C., Chang H. and Kim V.N. (2012) Mono-uridylation of pre-MicroRNA as a key step in the biogenesis of group II let-7 MicroRNAs. Cell, 151, 521-532
7. Jones M.R., Quinton L.J., Blahna M.T., Neilson J.R., Fu S., Ivanov A.R., Wolf D.A. and Mizgerd J.P. (2009) Zcchc11-dependent uridylation of microRNA directs cytokine expression. Nat. Cell Biol, 11, 1157-1163
8. Jones M.R., Blahna M.T., Kozlowski E., Matsuura K.Y., Ferrari J.D., Morris S.A., Powers J.T., Daley G.Q., Quinton L.J. and Mizgerd J.P. (2012) Zcchc11 Uridylates Mature miRNAs to Enhance Neonatal IGF-1 Expression, Growth, and Survival. PLoS Genet., 8, e1003105
9. van Wolfswinkel J.C., Claycomb J.M., Batista P.J., Mello C.C., Berezikov E. and Ketting R.F. (2009) CDE-1 affects chromosome segregation through uridylation of CSR-1-bound siRNAs. Cell, 139, 135-148
10. Ibrahim F., Rymarquis L.A., Kim E.J., Becker J., Balassa E., Green P.J. and Cerutti H. (2010) Uridylation of mature miRNAs and siRNAs by the MUT68 nucleotidyltransferase promotes their degradation in Chlamydomonas. Proc. Natl Acad. Sci. USA, 107, 3906-3911
11. Kamminga L.M., Luteijn M.J., den Broeder M.J., Redl S., Kaaij L.J., Roovers E.F., Ladurner P., Berezikov E. and Ketting R.F. (2010) Hen1 is required for oocyte development and piRNA stability in zebrafish. EMBO J., 29, 3688-3700
12. Ren G., Chen X. and Yu B. (2012) Uridylation of miRNAs by HEN1 SUPPRESSOR1 in Arabidopsis. Curr. Biol., 22, 695-700
13. Zhao Y., Yu Y., Zhai J., Ramachandran V., Dinh T.T., Meyers B.C., Mo B. and Chen X. (2012) The arabidopsis nucleotidyl transferase HESO1 uridylates unmethylated small RNAs to trigger their degradation. Curr. Biol., 22, 689-694
14. Yu B., Yang Z., Li J., Minakhina S., Yang M., Padgett R.W., Steward R. and Chen X. (2005) Methylation as a crucial step in plant microRNA biogenesis. Science, 307, 932-935
15. Li J., Yang Z., Yu B., Liu J. and Chen X. (2005) Methylation protects miRNAs and siRNAs from a 30-end uridylation activity in Arabidopsis. Curr. Biol., 15, 1501-1507
16. Hoefig K.P., Rath N., Heinz G.A., Wolf C., Dameris J., Schepers A., Kremmer E., Ansel K.M. and Heissmeyer V. (2012) Eri1 degrades the stem-loop of oligouridylated histone mRNAs to induce replication-dependent decay. Nat. Struct. Mol. Biol., 20, 73-81
17. Shen B. and Goodman H.M. (2004) Uridine addition after microRNA-directed cleavage. Science, 306, 997
18. Song M.G. and Kiledjian M. (2007) 30 Terminal oligo U-Tractmediated stimulation of decapping. RNA, 13, 2356-2365
19. Mullen T.E. and Marzluff W.F. (2008) Degradation of histone mRNA requires oligouridylation followed by decapping and simultaneous degradation of the mRNA both 50 to 30 and 30 to 50. Genes Dev., 22, 50-65
20. Rissland O.S. and Norbury C.J. (2009) Decapping is preceded by 30 uridylation in a novel pathway of bulk mRNA turnover. Nat. Struct. Mol. Biol., 16, 616-623
21. Morozov I.Y., Jones M.G., Razak A.A., Rigden D.J. and Caddick M.X. (2010) CUCU modification of mRNA promotes decapping and transcript degradation in Aspergillus nidulans. Mol. Cell. Biol., 30, 460-469
22. Morozov I.Y., Jones M.G., Gould P.D., Crome V., Wilson J.B., Hall A.J., Rigden D.J. and Caddick M.X. (2012) mRNA 30 tagging is induced by nonsense-mediated decay and promotes ribosome dissociation. Mol. Cell. Biol., 32, 2585-2595
23. Kwak J.E. and Wickens M. (2007) A family of poly(U) polymerases. RNA, 13, 860-867
24. Gazzani S., Lawrenson T., Woodward C., Headon D. and Sablowski R. (2004) A link between mRNA turnover and RNA interference in Arabidopsis. Science, 306, 1046-1048
25. Rissland O.S., Mikulasova A. and Norbury C.J. (2007) Efficient RNA polyuridylation by noncanonical poly(A) polymerases. Mol. Cell. Biol., 27, 3612-3624
26. Sement F.M. and Gagliardi D. (2013) Polydenylation: Methods and Protocols. In: Rorbach J. (ed). Methods In Molecular Biology. Humana Press, Springer Science, in press
27. Mustroph A., Juntawong P. and Bailey-Serres J. (2009) Isolation of plant polysomal mRNA by differential centrifugation and ribosome immunopurification methods. Methods Mol. Biol., 553, 109-126
28. Munoz-Tello P., Gabus C. and Thore S. (2012) Functional implications from the Cid1 poly(U) polymerase crystal structure. Structure, 20, 977-986
29. Lunde B.M., Magler I. and Meinhart A. (2012) Crystal structures of the Cid1 poly (U) polymerase reveal the mechanism for UTP selectivity. Nucleic Acids Res., 40, 9815-9824
30. Yates L.A., Fleurdepine S., Rissland O.S., De Colibus L., Harlos K., Norbury C.J. and Gilbert R.J. (2012) Structural basis for the activity of a cytoplasmic RNA terminal uridylyl transferase. Nat. Struct. Mol. Biol., 19, 782-787
31. Xu J., Yang J.Y., Niu Q.W. and Chua N.H. (2006) Arabidopsis DCP2, DCP1, and VARICOSE form a decapping complex required for postembryonic development. Plant Cell, 18, 3386-3398
32. Weber C., Nover L. and Fauth M. (2008) Plant stress granules and mRNA processing bodies are distinct from heat stress granules. Plant J., 56, 517-530
33. Narsai R., Howell K.A., Millar A.H., O'Toole N., Small I. and Whelan J. (2007) Genome-wide analysis of mRNA decay rates and their determinants in Arabidopsis thaliana. Plant Cell, 19, 3418-3436
34. Kastenmayer J.P. and Green P.J. (2000) Novel features of the XRN-family in Arabidopsis: Evidence that AtXRN4, one of several orthologs of nuclear Xrn2p/Rat1p, functions in the cytoplasm. Proc. Natl Acad. Sci. USA, 97, 13985-13990
35. Potuschak T., Vansiri A., Binder B.M., Lechner E., Vierstra R.D. and Genschik P. (2006) The exoribonuclease XRN4 is a component of the ethylene response pathway in Arabidopsis. Plant Cell, 18, 3047-3057
36. Olmedo G., Guo H., Gregory B.D., Nourizadeh S.D., Aguilar-Henonin L., Li H., An F., Guzman P. and Ecker J.R. (2006) ETHYLENE-INSENSITIVE5 encodes a 50->30 exoribonuclease required for regulation of the EIN3-Targeting F-box proteins EBF1/2. Proc. Natl Acad. Sci. USA, 103, 13286-13293
37. Goeres D.C., Van Norman J.M., Zhang W., Fauver N.A., Spencer M.L. and Sieburth L.E. (2007) Components of the Arabidopsis mRNA decapping complex are required for early seedling development. Plant Cell, 19, 1549-1564
38. Rymarquis L.A., Souret F.F. and Green P.J. (2011) Evidence that XRN4, an Arabidopsis homolog of exoribonuclease XRN1, preferentially impacts transcripts with certain sequences or in particular functional categories. RNA, 17, 501-511
39. Gregory B.D., O'Malley R.C., Lister R., Urich M.A., Tonti-Filippini J., Chen H., Millar A.H. and Ecker J.R. (2008) A link between RNA metabolism and silencing affecting Arabidopsis development. Dev. Cell, 14, 854-866
40. Sachs A.B., Davis R.W. and Kornberg R.D. (1987) A single domain of yeast poly(A)-binding protein is necessary and sufficient for RNA binding and cell viability. Mol. Cell. Biol., 7, 3268-3276
41. Sherstnev A., Duc C., Cole C., Zacharaki V., Hornyik C., Ozsolak F., Milos P.M., Barton G.J. and Simpson G.G. (2012) Direct sequencing of Arabidopsis thaliana RNA reveals patterns of cleavage and polyadenylation. Nat. Struct. Mol .Biol., 19, 845-852
42. Hu W., Sweet T.J., Chamnongpol S., Baker K.E. and Coller J. (2009) Co-Translational mRNA decay in Saccharomyces cerevisiae. Nature, 461, 225-229
43. Beggs J.D. (2005) Lsm proteins and RNA processing. Biochem. Soc. Trans., 33, 433-438
44. Bouveret E., Rigaut G., Shevchenko A., Wilm M. and Seraphin B. (2000) A Sm-like protein complex that participates in mRNA degradation. EMBO J., 19, 1661-1671
45. Tharun S. (2009) Roles of eukaryotic Lsm proteins in the regulation of mRNA function. Int. Rev. Cell. Mol. Biol., 272, 149-189
46. Haas G., Braun J.E., Igreja C., Tritschler F., Nishihara T. and Izaurralde E. (2010) HPat provides a link between deadenylation and decapping in metazoa. J. Cell Biol., 189, 289-302
47. Ozgur S., Chekulaeva M. and Stoecklin G. (2010) Human Pat1b connects deadenylation with mRNA decapping and controls the assembly of processing bodies. Mol. Cell. Biol., 30, 4308-4323
48. Coller J. and Parker R. (2005) General translational repression by activators of mRNA decapping. Cell, 122, 875-886
49. Boeck R., Lapeyre B., Brown C.E. and Sachs A.B. (1998) Capped mRNA degradation intermediates accumulate in the yeast spb8-2 mutant. Mol. Cell. Biol., 18, 5062-5072
50. He W. and Parker R. (2001) The yeast cytoplasmic LsmI/Pat1p complex protects mRNA 30 termini from partial degradation. Genetics, 158, 1445-1455
51. Tharun S. (2009) Lsm1-7-Pat1 complex: A link between 30 and 50-ends in mRNA decay? RNA Biol., 6, 228-232
52. Lange H., Holec S., Cognat V., Pieuchot L., Le Ret M., Canaday J. and Gagliardi D. (2008) Degradation of a polyadenylated rRNA maturation by-product involves one of the three RRP6-like proteins in Arabidopsis thaliana. Mol. Cell. Biol., 28, 3038-3044
53. Zhang W., Murphy C. and Sieburth L.E. (2010) Conserved RNaseII domain protein functions in cytoplasmic mRNA decay and suppresses Arabidopsis decapping mutant phenotypes. Proc. Natl Acad. Sci. USA, 107, 15981-15985
54. Boyes D.C., Zayed A.M., Ascenzi R., McCaskill A.J., Hoffman N.E., Davis K.R. and Gorlach J. (2001) Growth stagebased phenotypic analysis of Arabidopsis: A model for high throughput functional genomics in plants. Plant Cell, 13, 1499-1510
55. Lurin C., Andres C., Aubourg S., Bellaoui M., Bitton F., Bruyere C., Caboche M., Debast C., Gualberto J., Hoffmann B. et al. (2004) Genome-wide analysis of Arabidopsis pentatricopeptide repeat proteins reveals their essential role in organelle biogenesis. Plant Cell, 16, 2089-2103
56. Yang Y.H., Dudoit S., Luu P., Lin D.M., Peng V., Ngai J. and Speed T.P. (2002) Normalization for cDNA microarray data: A robust composite method addressing single and multiple slide systematic variation. Nucleic Acids Res., 30, e15
57. Smyth G.K. (2004) Linear models and empirical bayes methods for assessing differential expression in microarray experiments. Stat. Appl. Genet. Mol. Biol., 3, Article3
58. Storey J.D. and Tibshirani R. (2003) Statistical significance for genomewide studies. Proc. Natl Acad. Sci. USA, 100, 9440-9445
59. Provart N. and Zhu T. (2003) A Browser-based functional classification superviewer for Arabidopsis genomics. Curr. Comput. Mol. Biol., 2003, 271-272
60. Maere S., Heymans K. and Kuiper M. (2005) BiNGO: A cytoscape plugin to assess overrepresentation of gene ontology categories in biological networks. Bioinformatics, 21, 3448-3449
61. Gagnot S., Tamby J.P., Martin-Magniette M.L., Bitton F., Taconnat L., Balzergue S., Aubourg S., Renou J.P., Lecharny A. and Brunaud V. (2008) CATdb: A public access to Arabidopsis transcriptome data from the URGV-CATMA platform. Nucleic Acids Res., 36, D986-D990