Small RNAs derived from the 5′ end of tRNAs can inhibit protein translation in human cells

RNA Biology

Volumn 10, Issue 4, 2013, Pages 553-563

  Sobala, Andrew ^a,c   Hutvagner, Gyorgy ^a,b  

^a UNIVERSITY OF DUNDEE   (United Kingdom)

^b UNIVERSITY OF TECHNOLOGY SYDNEY   (Australia)

^c GUY S HOSPITAL   (United Kingdom)

Author keywords

Short tRNA fragment; Small RNA; Translation repression; tRF; tRNA

Indexed keywords

DINUCLEOTIDE; MESSENGER RNA; POLYADENYLIC ACID BINDING PROTEIN; RENILLA LUCIFERIN 2 MONOOXYGENASE; TRANSFER RNA;

ARTICLE; CELL PROLIFERATION; CELL STRESS; CONTROLLED STUDY; ENZYME ACTIVITY; GENE CONTROL; GENE EXPRESSION; GENETIC TRANSFECTION; HELA CELL; HUMAN; HUMAN CELL; NONHUMAN; NUCLEOTIDE SEQUENCE; PHYSIOLOGICAL STRESS; PROTEIN RNA BINDING; RENILLA; TRANSLATION INITIATION;

EID: 84879025267     PISSN: 15476286     EISSN: 15558584     Source Type: Journal    
DOI: 10.4161/rna.24285     Document Type: Article

References (39)

1. Farazi TA, Juranek SA, Tuschl T. The growing catalog of small RNAs and their association with distinct Argonaute/Piwi family members. Development 2008; 135:1201-14; PMID:18287206; http://dx.doi.org/10.1242/dev.005629.
2. Bernstein E, Caudy AA, Hammond SM, Hannon GJ. Role for a bidentate ribonuclease in the initiation step of RNA interference. Nature 2001; 409:363-6; PMID:11201747; http://dx.doi.org/10.1038/35053110.
3. Hutvágner G, McLachlan J, Pasquinelli AE, Bálint E, Tuschl T, Zamore PD. A cellular function for the RNA-interference enzyme Dicer in the maturation of the let-7 small temporal RNA. Science 2001; 293:834-8; PMID:11452083; http://dx.doi.org/10.1126/science.1062961.
4. Brennecke J, Aravin AA, Stark A, Dus M, Kellis M, Sachidanandam R, et al. Discrete small RNA-generating loci as master regulators of transposon activity in Drosophila. Cell 2007; 128:1089-103; PMID:17346786; http://dx.doi.org/10. 1016/j.cell.2007.01.043.
5. Meister G, Landthaler M, Patkaniowska A, Dorsett Y, Teng G, Tuschl T. Human Argonaute2 mediates RNA cleavage targeted by miRNAs and siRNAs. Mol Cell 2004; 15:185-97; PMID:15260970; http://dx.doi.org/10.1016/j.molcel.2004.07.007.
6. Liu J, Carmell MA, Rivas FV, Marsden CG, Thomson JM, Song JJ, et al. Argonaute2 is the catalytic engine of mammalian RNAi. Science 2004; 305:1437-41; PMID:15284456; http://dx.doi.org/10.1126/science.1102513.
7. Pillai RS, Artus CG, Filipowicz W. Tethering of human Ago proteins to mRNA mimics the miRNA-mediated repression of protein synthesis. RNA 2004; 10:1518-25; PMID:15337849; http://dx.doi.org/10.1261/rna.7131604.
8. Ender C, Krek A, Friedländer MR, Beitzinger M, Weinmann L, Chen W, et al. A human snoRNA with microRNA-like functions. Mol Cell 2008; 32:519-28; PMID:19026782; http://dx.doi.org/10.1016/j.molcel.2008.10.017.
9. Bühler M, Spies N, Bartel DP, Moazed D. TRAMP-mediated RNA surveillance prevents spurious entry of RNAs into the Schizosaccharomyces pombe siRNA pathway. Nat Struct Mol Biol 2008; 15:1015-23; PMID:18776903; http://dx.doi.org/10.1038/nsmb.1481.
10. Kawaji H, Nakamura M, Takahashi Y, Sandelin A, Katayama S, Fukuda S, et al. Hidden layers of human small RNAs. BMC Genomics 2008; 9:157; PMID:18402656; http://dx.doi.org/10.1186/1471-2164-9-157.
11. Babiarz JE, Ruby JG, Wang Y, Bartel DP, Blelloch R. Mouse ES cells express endogenous shRNAs, siRNAs, and other Microprocessor-independent, Dicer-dependent small RNAs. Genes Dev 2008; 22:2773-85; PMID:18923076; http://dx.doi.org/10.1101/gad.1705308.
12. Cole C, Sobala A, Lu C, Thatcher SR, Bowman A, Brown JW, et al. Filtering of deep sequencing data reveals the existence of abundant Dicer-dependent small RNAs derived from tRNAs. RNA 2009; 15:2147-60; PMID:19850906; http://dx.doi.org/10.1261/rna.1738409.
13. Yeung ML, Bennasser Y, Watashi K, Le SY, Houzet L, Jeang KT. Pyrosequencing of small non-coding RNAs in HIV-1 infected cells: evidence for the processing of a viral-cellular double-stranded RNA hybrid. Nucleic Acids Res 2009; 37:6575-86; PMID:19729508; http://dx.doi.org/10.1093/nar/gkp707.
14. Lee YS, Shibata Y, Malhotra A, Dutta A. A novel class of small RNAs: tRNA-derived RNA fragments (tRFs). Genes Dev 2009; 23:2639-49; PMID:19933153; http://dx.doi.org/10.1101/gad.1837609.
15. Hsieh LC, Lin SI, Shih ACC, Chen JW, Lin WY, Tseng CY, et al. Uncovering small RNA-mediated responses to phosphate deficiency in Arabidopsis by deep sequencing. Plant Physiol 2009; 151:2120-32; PMID:19854858; http://dx.doi.org/ 10.1104/pp.109.147280.
16. Liao JY, Ma LM, Guo YH, Zhang YC, Zhou H, Shao P, et al. Deep sequencing of human nuclear and cytoplasmic small RNAs reveals an unexpectedly complex subcellular distribution of miRNAs and tRNA 3' trailers. PLoS One 2010; 5:e10563; PMID:20498841; http://dx.doi.org/10.1371/journal.pone.0010563.
17. Haussecker D, Huang Y, Lau A, Parameswaran P, Fire AZ, Kay MA. Human tRNA-derived small RNAs in the global regulation of RNA silencing. RNA 2010; 16:673-95; PMID:20181738; http://dx.doi.org/10.1261/rna.2000810.
18. Couvillion MT, Sachidanandam R, Collins K. A growth-essential Tetrahymena Piwi protein carries tRNA fragment cargo. Genes Dev 2010; 24:2742-7; PMID:21106669; http://dx.doi.org/10.1101/gad.1996210.
19. Yamasaki S, Ivanov P, Hu GF, Anderson P. Angiogenin cleaves tRNA and promotes stress-induced translational repression. J Cell Biol 2009; 185:35-42; PMID:19332886; http://dx.doi.org/10.1083/jcb.200811106.
20. Li Z, Ender C, Meister G, Moore PS, Chang Y, John B. Extensive terminal and asymmetric processing of small RNAs from rRNAs, snoRNAs, snRNAs, and tRNAs. Nucleic Acids Res 2012; 40:6787-99; PMID:22492706; http://dx.doi.org/10.1093/ nar/gks307.
21. Pederson T. Regulatory RNAs derived from transfer RNA? RNA 2010; 16:1865-9; PMID:20719919; http://dx.doi.org/10.1261/rna.2266510.
22. Sobala A, Hutvagner G. Transfer RNA-derived fragments: origins, processing, and functions. Wiley Interdiscip Rev RNA 2011; 2:853-62; PMID:21976287; http://dx.doi.org/10.1002/wrna.96.
23. Maute RL, Schneider C, Sumazin P, Holmes A, Califano A, Basso K, et al. tRNA-derived microRNA modulates proliferation and the DNA damage response and is down-regulated in B cell lymphoma. Proc Natl Acad Sci USA 2013; 110:1404-9; PMID:23297232; http://dx.doi.org/10.1073/pnas.1206761110.
24. Lee SR, Collins K. Starvation-induced cleavage of the tRNA anticodon loop in Tetrahymena thermophila. J Biol Chem 2005; 280:42744-9; PMID:16272149; http://dx.doi.org/10.1074/jbc.M510356200.
25. Thompson DM, Lu C, Green PJ, Parker R. tRNA cleavage is a conserved response to oxidative stress in eukaryotes. RNA 2008; 14:2095-103; PMID:18719243; http://dx.doi.org/10.1261/rna.1232808.
26. Emara MM, Ivanov P, Hickman T, et al. Angiogenin-induced tiRNAs promote stress-induced stress granule assembly. J Biol Chem 2010; 285:10959-68; PMID:20129916; http://dx.doi.org/10.1074/jbc.M109.077560.
27. Ivanov P, Emara MM, Villen J, Gygi SP, Anderson P. Angiogenin-induced tRNA fragments inhibit translation initiation. Mol Cell 2011; 43:613-23; PMID:21855800; http://dx.doi.org/10.1016/j.molcel.2011.06.022.
28. Schwarz DS, Hutvágner G, Haley B, Zamore PD. Evidence that siRNAs function as guides, not primers, in the Drosophila and human RNAi pathways. Mol Cell 2002; 10:537-48; PMID:12408822; http://dx.doi.org/10.1016/S1097-2765(02) 00651-2.
29. Hutvágner G, Simard MJ, Mello CC, Zamore PD. Sequence-specific inhibition of small RNA function. PLoS Biol 2004; 2:E98; PMID:15024405; http://dx.doi.org/10.1371/journal.pbio.0020098.
30. Bergamini G, Preiss T, Hentze MW. Picornavirus IRESes and the poly(A) tail jointly promote cap-independent translation in a mammalian cell-free system. RNA 2000; 6:1781-90; PMID:11142378; http://dx.doi.org/10.1017/ S1355838200001679.
31. Rehmsmeier M, Steffen P, Hochsmann M, Giegerich R. Fast and effective prediction of microRNA/target duplexes. RNA 2004; 10:1507-17; PMID:15383676; http://dx.doi.org/10.1261/rna.5248604.
32. Marck C, Grosjean H. tRNomics: analysis of tRNA genes from 50 genomes of Eukarya, Archaea, and Bacteria reveals anticodon-sparing strategies and domain-specific features. RNA 2002; 8:1189-232; PMID:12403461; http://dx.doi.org/10.1017/S1355838202022021.
33. Huntzinger E, Izaurralde E. Gene silencing by microRNAs: contributions of translational repression and mRNA decay. Nat Rev Genet 2011; 12:99-110; PMID:21245828; http://dx.doi.org/10.1038/nrg2936.
34. Varshney U, Lee CP, RajBhandary UL. Direct analysis of aminoacylation levels of tRNAs in vivo. Application to studying recognition of Escherichia coli initiator tRNA mutants by glutaminyl-tRNA synthetase. J Biol Chem 1991; 266:24712-8; PMID:1761566.
35. Tarun SZ Jr., Sachs AB. Binding of eukaryotic translation initiation factor 4E (eIF4E) to eIF4G represses translation of uncapped mRNA. Mol Cell Biol 1997; 17:6876-86; PMID:9372919.
36. Gebetsberger J, Zywicki M, Künzi A, Polacek N. tRNA-derived fragments target the ribosome and function as regulatory non-coding RNA in Haloferax volcanii. Archaea 2012; 2012:260909; PMID:23326205; http://dx.doi.org/10.1155/2012/260909.
37. Netzer N, Goodenbour JM, David A, Dittmar KA, Jones RB, Schneider JR, et al. Innate immune and chemically triggered oxidative stress modifies translational fidelity. Nature 2009; 462:522-6; PMID:19940929; http://dx.doi.org/10.1038/nature08576.
38. Silvera D, Formenti SC, Schneider RJ. Translational control in cancer. Nat Rev Cancer 2010; 10:254-66; PMID:20332778; http://dx.doi.org/10.1038/ nrc2824.
39. Zuker M. Mfold web server for nucleic acid folding and hybridization prediction. Nucleic Acids Res 2003; 31:3406-15; PMID:12824337; http://dx.doi.org/10.1093/nar/gkg595.