The role of wobble uridine modifications in +1 translational frameshifting in eukaryotes

Nucleic Acids Research

Volumn 43, Issue 19, 2015, Pages 9489-9499

  Tükenmez, Hasan ^a   Xu, Hao ^a   Esberg, Anders ^a   Byström, Anders S ^a  

^a UMEÅ UNIVERSITY   (Sweden)

Author keywords

[No Author keywords available]

Indexed keywords

5 CARBAMOYLMETHYL 2' O METHYLURIDINE; 5 CARBAMOYLMETHYLURIDINE; 5 METHOXYCARBONYLMETHYL 2 THIOURIDINE; 5 METHOXYCARBONYLMETHYLURIDINE; BETA GALACTOSIDASE; GUANOSINE TRIPHOSPHATE; MESSENGER RNA; NUCLEOSIDE; SULFUR; TRANSFER RNA; UNCLASSIFIED DRUG; URIDINE; 5-CARBOMETHOXYMETHYL-2-THIOURIDINE; ANTICODON; FUNGAL RNA; THIOURIDINE;

ANTICODON; ARTICLE; CODON; CONTROLLED STUDY; EUKARYOTE; FRAMESHIFT MUTATION; NONHUMAN; PHENOTYPE; PLEIOTROPY; PRIORITY JOURNAL; RENILLA; RIBOSOMAL FRAMESHIFTING; RNA TRANSLATION; SACCHAROMYCES CEREVISIAE; ANALOGS AND DERIVATIVES; CHEMISTRY; GENETICS; METABOLISM;

ANTICODON; FRAMESHIFTING, RIBOSOMAL; RNA, FUNGAL; RNA, TRANSFER; SACCHAROMYCES CEREVISIAE; THIOURIDINE; URIDINE;

EID: 84952048527     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gkv832     Document Type: Article

References (58)

1. Kurland,C.G. (1992) Translational accuracy and the fitness of bacteria. Annu. Rev. Genet., 26, 29-50.
2. Parker,J. (1989) Errors and alternatives in reading the universal genetic code. Microbiol. Rev., 53, 273-298.
3. Atkins,J.F. and Björk,G.R. (2009) A gripping tale of ribosomal frameshifting: extragenic suppressors of frameshift mutations spotlight P-site realignment. Microbiol. Mol. Biol. Rev.: MMBR, 73, 178-210.
4. Björk,G.R. and Hagervall,T.G. (2014) Transfer RNA Modification: Presence, Synthesis, and Function. EcoSal Plus, doi:10.1128/ecosalplus.ESP-0007-2013.
5. Björk,G.R., Wikström,P.M. and Byström,A.S. (1989) Prevention of translational frameshifting by the modified nucleoside 1-methylguanosine. Science,244, 986-989.
6. Urbonavièius,J., Qian,Q., Durand,J.M., Hagervall,T.G. and Björk,G.R. (2001) Improvement of reading frame maintenance is a common function for several tRNA modifications. EMBO J., 20, 4863-4873.
7. Carlson,B.A., Kwon,S.Y., Chamorro,M., Oroszlan,S., Hatfield,D.L. and Lee,B.J. (1999) Transfer RNA modification status influences retroviral ribosomal frameshifting. Virology, 255, 2-8.
8. Carlson,B.A., Mushinski,J.F., Henderson,D.W., Kwon,S.Y., Crain,P.F., Lee,B.J. and Hatfield,D.L. (2001) 1-Methylguanosine in place of Y base at position 37 in phenylalanine tRNA is responsible for its shiftiness in retroviral ribosomal frameshifting. Virology, 279, 130-135.
9. Waas,W.F., Druzina,Z., Hanan,M. and Schimmel,P. (2007) Role of a tRNA base modification and its precursors in frameshifting in eukaryotes. J. Biol. Chem., 282, 26026-26034.
10. Lecointe,F., Namy,O., Hatin,I., Simos,G., Rousset,J.P. and Grosjean,H. (2002) Lack of pseudouridine 38/39 in the anticodon arm of yeast cytoplasmic tRNA decreases in vivo recoding efficiency. J. Biol. Chem., 277, 30445-30453.
11. Lin,C.A., Ellis,S.R. and True,H.L. (2010) The Sua5 protein is essential for normal translational regulation in yeast. Mol. Cell. Biol., 30, 354-363.
12. El Yacoubi,B., Hatin,I., Deutsch,C., Kahveci,T., Rousset,J.P., Iwata-Reuyl,D., Murzin,A.G. and de Crécy-Lagard,V. (2011) A role for the universal Kae1/Qri7/YgjD (COG0533) family in tRNA modification. EMBO J., 30, 882-893.
13. Miyauchi,K., Kimura,S. and Suzuki,T. (2013) A cyclic form of N6-threonylcarbamoyladenosine as a widely distributed tRNA hypermodification. Nat. Chem. Biol., 9, 105-111.
14. Brierley,I., Meredith,M.R., Bloys,A.J. and Hagervall,T.G. (1997) Expression of a coronavirus ribosomal frameshift signal in Escherichia coli: influence of tRNA anticodon modification on frameshifting. J. Mol. Biol., 270, 360-373.
15. Licznar,P., Mejlhede,N., Prère,M.F., Wills,N., Gesteland,R.F., Atkins,J.F. and Fayet,O. (2003) Programmed translational -1 frameshifting on hexanucleotide motifs and the wobble properties of tRNAs. EMBO J., 22, 4770-4778.
16. Urbonavièius,J., Stahl,G., Durand,J.M., Ben Salem,S.N., Qian,Q., Farabaugh,P.J. and Björk,G.R. (2003) Transfer RNA modifications that alter +1 frameshifting in general fail to affect -1 frameshifting. RNA,9, 760-768.
17. Maynard,N.D., Macklin,D.N., Kirkegaard,K. and Covert,M.W. (2012) Competing pathways control host resistance to virus via tRNA modification and programmed ribosomal frameshifting. Mol. Syst. Biol., 8, 567-579.
18. Farabaugh,P.J. (1996) Programmed translational frameshifting. Microbiol. Rev., 60, 103-134.
19. Farabaugh,P.J. (1996) Programmed translational frameshifting. Annu. Revi. Genet., 30, 507-528.
20. Björk,G.R., Durand,J.M., Hagervall,T.G., Leipuvienė,R., Lundgren,H.K., Nilsson,K., Chen,P., Qian,Q. and Urbonavičius,J. (1999) Transfer RNA modification: influence on translational frameshifting and metabolism. FEBS Lett., 452, 47-51.
21. Farabaugh,P.J. and Björk,G.R. (1999) How translational accuracy influences reading frame maintenance. EMBO J., 18, 1427-1434.
22. Gallant,J., Lindsley,D. and Masucci,J. (2000) The unbearable lightness of peptidyl-tRNA. Ribosome: Struct. Func. Antibiot. Cell. Interact., 385-396.
23. Näsvall,S.J., Nilsson,K. and Björk,G.R. (2009) The ribosomal grip of the peptidyl-tRNA is critical for reading frame maintenance. J. Mol. Biol., 385, 350-367.
24. Jäger,G., Nilsson,K. and Björk,G.R. (2013) The phenotype of many independently isolated +1 frameshift suppressor mutants supports a pivotal role of the P-site in reading frame maintenance. PloS One, 8, e60246.
25. Glasser,A.L., El Adlouni,C., Keith,G., Sochacka,E., Malkiewicz,A., Santos,M., Tuite,M.F. and Desgrès,J. (1992) Presence and coding properties of 2′-O-methyl-5-carbamoylmethyluridine (ncm5Um) in the wobble position of the anticodon of tRNA(Leu) (U∗AA) from brewer's yeast. FEBS Lett., 314, 381-385.
26. Johansson,M.J., Esberg,A., Huang,B., Björk,G.R. and Byström,A.S. (2008) Eukaryotic wobble uridine modifications promote a functionally redundant decoding system. Mol. Cell. Biol., 28, 3301-3312.
27. Keith,G., Desgrès,J., Pochart,P., Heyman,T., Kuo,K.C. and Gehrke,C.W. (1990) Eukaryotic tRNAs(Pro): primary structure of the anticodon loop; presence of 5-carbamoylmethyluridine or inosine as the first nucleoside of the anticodon. Biochim. Biophys. Acta., 1049, 255-260.
28. Kobayashi,T., Irie,T., Yoshida,M., Takeishi,K. and Ukita,T. (1974) The primary structure of yeast glutamic acid tRNA specific to the GAA codon. Biochim. Biophys. Acta., 366, 168-181.
29. Kuntzel,B., Weissenbach,J., Wolff,R.E., Tumaitis-Kennedy,T.D., Lane,B.G. and Dirheimer,G. (1975) Presence of the methylester of 5-carboxymethyl uridine in the wobble position of the anticodon of tRNAIII Arg from brewer's yeast. Biochimie, 57, 61-70.
30. Lu,J., Huang,B., Esberg,A., Johansson,M.J. and Byström,A.S. (2005) The Kluyveromyces lactis γ-toxin targets tRNA anticodons. RNA, 11, 1648-1654.
31. Smith,C.J., Teh,H.S., Ley,A.N. and D'Obrenan,P. (1973) The nucleotide sequences and coding properties of the major and minor lysine transfer ribonucleic acids from the haploid yeast Saccharomyces cerevisiae S288C. J. Biol. Chem., 248, 4475-4485.
32. Yamamoto,N., Yamaizumi,Z., Yokoyama,S., Miyazawa,T. and Nishimura,S. (1985) Modified nucleoside, 5-carbamoylmethyluridine, located in the first position of the anticodon of yeast valine tRNA. J. Biochem. (Tokyo), 97, 361-364.
33. Karlsborn,T., Tükenmez,H., Mahmud,A.K., Xu,F., Xu,H. and Byström,A.S. (2014) Elongator, a conserved complex required for wobble uridine modifications in Eukaryotes. RNA Biol., 11, 1519-1528.
34. Esberg,A., Huang,B., Johansson,M.J.O. and Byström,A.S. (2006) Elevated Levels of Two tRNA Species Bypass the Requirement for Elongator Complex in Transcription and Exocytosis. Mol. Cell., 24, 139-148.
35. Chen,C., Huang,B., Eliasson,M., Rydén,P. and Byström,A.S. (2011) Elongator complex influences telomeric gene silencing and DNA damage response by its role in wobble uridine tRNA modification. PLoS Genet., 7, e1002258.
36. Näsvall,S.J., Chen,P. and Björk,G.R. (2004) The modified wobble nucleoside uridine-5-oxyacetic acid in tRNAPro(cmo5UGG) promotes reading of all four proline codons in vivo. RNA, 10, 1662-1673.
37. Patil,A., Chan,C.T., Dyavaiah,M., Rooney,J.P., Dedon,P.C. and Begley,T.J. (2012) Translational infidelity-induced protein stress results from a deficiency in Trm9-catalyzed tRNA modifications. RNA Biol., 9, 990-1001.
38. Gietz,D., St Jean,A., Woods,R.A. and Schiestl,R.H. (1992) Improved method for high efficiency transformation of intact yeast cells. Nucleic Acids Res., 20, 1425.
39. Burke,D., Dawson,D. and Stearns,T. (2000) Methods in yeast genetics. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
40. Harger,J.W. and Dinman,J.D. (2003) An in vivo dual-luciferase assay system for studying translational recoding in the yeast Saccharomyces cerevisiae. RNA, 9, 1019-1024.
41. Belcourt,M.F. and Farabaugh,P.J. (1990) Ribosomal frameshifting in the yeast retrotransposon Ty: tRNAs induce slippage on a 7 nucleotide minimal site. Cell, 62, 339-352.
42. Rajbhandary,U.L., Chang,S.H., Stuart,A., Faulkner,R.D., Hoskinson,R.M. and Khorana,H.G. (1967) Studies on polynucleotides, lxviii the primary structure of yeast phenylalanine transfer RNA. Proc. Natl. Acad. Sci. U.S.A., 57, 751-758.
43. Jühling,F., Mörl,M., Hartmann,R.K., Sprinzl,M., Stadler,P.F. and Pütz,J. (2009) tRNAdb 2009: compilation of tRNA sequences and tRNA genes. Nucleic Acids Res., 37, D159-D162.
44. Kisselev,L.L. and Buckingham,R.H. (2000) Translational termination comes of age. Trends Biochem. Sci., 25, 561-566.
45. Huang,B., Johansson,M.J.O. and Byström,A.S. (2005) An early step in wobble uridine tRNA modification requires the Elongator complex. RNA, 11, 424-436.
46. Kalhor,H.R. and Clarke,S. (2003) Novel methyltransferase for modified uridine residues at the wobble position of tRNA. Mol. Cell. Biol., 23, 9283-9292.
47. Mazauric,M.H., Dirick,L., Purushothaman,S.K., Björk,G.R. and Lapeyre,B. (2010) Trm112p is a 15-kDa zinc finger protein essential for the activity of two tRNA and one protein methyltransferases in yeast. J. Biol. Chem., 285, 18505-18515.
48. Björk,G.R., Huang,B., Persson,O.P. and Byström,A.S. (2007) A conserved modified wobble nucleoside (mcm5s2U) in lysyl-tRNA is required for viability in yeast. RNA, 13, 1245-1255.
49. Fahlman,R.P., Dale,T. and Uhlenbeck,O.C. (2004) Uniform binding of aminoacylated transfer RNAs to the ribosomal A and P sites. Mol. Cell., 16, 799-805.
50. Percudani,R., Pavesi,A. and Ottonello,S. (1997) Transfer RNA gene redundancy and translational selection in Saccharomyces cerevisiae. J. Mol. Biol., 268, 322-330.
51. Rezgui,V.A., Tyagi,K., Ranjan,N., Konevega,A.L., Mittelstaet,J., Rodnina,M.V., Peter,M. and Pedrioli,P.G. (2013) tRNA tKUUU, tQUUG, and tEUUC wobble position modifications fine-tune protein translation by promoting ribosome A-site binding. Proc. Natl. Acad. Sci. U.S.A., 110, 12289-12294.
52. Fiorentini,P., Huang,K.N., Tishkoff,D.X., Kolodner,R.D. and Symington,L.S. (1997) Exonuclease I of Saccharomyces cerevisiae functions in mitotic recombination in vivo and in vitro. Mol. Cell. Biol., 17, 2764-2773.
53. Chen,C., Huang,B., Anderson,J.T. and Byström,A.S. (2011) Unexpected accumulation of ncm(5)U and ncm(5)S(2) (U) in a trm9 mutant suggests an additional step in the synthesis of mcm(5)U and mcm(5)S(2)U. PloS One, 6, e20783.
54. Madison,J.T. and Kung,H.K. (1967) Large oligonucleotides isolated from yeast tyrosine transfer ribonucleic acid after partial digestion with ribonuclease T1. J. Biol. Chem., 242, 1324-1330.
55. Nakai,Y., Nakai,M. and Hayashi,H. (2008) Thio-modification of yeast cytosolic tRNA requires a ubiquitin-related system that resembles bacterial sulfur transfer systems. J. Biol. Chem., 283, 27469-27476.
56. Leidel,S., Pedrioli,P.G., Bucher,T., Brost,R., Costanzo,M., Schmidt,A., Aebersold,R., Boone,C., Hofmann,K. and Peter,M. (2009) Ubiquitin-related modifier Urm1 acts as a sulphur carrier in thiolation of eukaryotic transfer RNA. Nature, 458, 228-232.
57. Noma,A., Sakaguchi,Y. and Suzuki,T. (2009) Mechanistic characterization of the sulfur-relay system for eukaryotic 2-thiouridine biogenesis at tRNA wobble positions. Nucleic Acids Res., 37, 1335-1352.
58. Farabaugh,P., Liao,X.B., Belcourt,M., Zhao,H., Kapakos,J. and Clare,J. (1989) Enhancer and silencerlike sites within the transcribed portion of a Ty2 transposable element of Saccharomyces cerevisiae. Mol. Cell. Biol., 9, 4824-4834.