S. cerevisiae Trm140 has two recognition modes for 3-methylcytidine modification of the anticodon loop of tRNA substrates

RNA

Volumn 23, Issue 3, 2017, Pages 406-419

  Han, Lu ^a   Marcus, Erin ^a   D'Silva, Sonia ^a   Phizicky, Eric M ^a  

^a UNIVERSITY OF ROCHESTER SCHOOL OF MEDICINE AND DENTISTRY   (United States)

Author keywords

3 methylcytidine; Anticodon loop; Methyltransferase; Modification; Specificity; tRNA

Indexed keywords

3 METHYLCYTIDINE; CYTIDINE DERIVATIVE; FUNGAL PROTEIN; SERINE TRANSFER RNA LIGASE; TRANSFER RNA; UNCLASSIFIED DRUG; 3-METHYLCYTIDINE; ABP140 PROTEIN, S CEREVISIAE; ACTIN BINDING PROTEIN; ANTICODON; CYTIDINE; PHENYLALANINE TRANSFER RNA; PROTEIN BINDING; RECOMBINANT PROTEIN; SACCHAROMYCES CEREVISIAE PROTEIN; SERINE TRANSFER RNA; THREONINE TRANSFER RNA; TRANSFER RNA METHYLTRANSFERASE;

AMINO TERMINAL SEQUENCE; ANIMAL; ANTICODON; ARTICLE; ASCOMYCETES; CARBOXY TERMINAL SEQUENCE; DNA FLANKING REGION; ESCHERICHIA COLI; FUNGUS GROWTH; IMMUNOBLOTTING; IN VITRO STUDY; NONHUMAN; PRIORITY JOURNAL; PROTEIN PURIFICATION; PROTEIN SECONDARY STRUCTURE; SACCHAROMYCES CEREVISIAE; SCHIZOSACCHAROMYCES POMBE; ANALOGS AND DERIVATIVES; BINDING SITE; CHEMISTRY; CONFORMATION; ENZYME SPECIFICITY; GENE EXPRESSION; GENETICS; METABOLISM; MOLECULAR CLONING; NUCLEOTIDE SEQUENCE; PROTEIN DOMAIN; PROTEIN SYNTHESIS;

ANTICODON; BASE SEQUENCE; BINDING SITES; CLONING, MOLECULAR; CYTIDINE; ESCHERICHIA COLI; GENE EXPRESSION; MICROFILAMENT PROTEINS; NUCLEIC ACID CONFORMATION; PROTEIN BINDING; PROTEIN BIOSYNTHESIS; PROTEIN DOMAINS; RECOMBINANT PROTEINS; RNA, TRANSFER, PHE; RNA, TRANSFER, SER; RNA, TRANSFER, THR; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; SUBSTRATE SPECIFICITY; TRNA METHYLTRANSFERASES;

EID: 85015162458     PISSN: 13558382     EISSN: 14699001     Source Type: Journal    
DOI: 10.1261/rna.059667.116     Document Type: Article

References (68)

1. Ser: sequence elements necessary for serylation and maturation of a tRNA with a long extra arm. EMBO J 12: 3333-3338.
2. Agris PF, Vendeix FA, Graham WD. 2007. tRNA's wobble decoding of the genome: 40 years of modification. J Mol Biol 366: 1-13.
3. Alexandrov A, Chernyakov I, Gu W, Hiley SL, Hughes TR, Grayhack EJ, Phizicky EM. 2006. Rapid tRNA decay can result from lack of non-essential modifications. Mol Cell 21: 87-96.
4. 6-isopen-tenylation of A37. RNA 22: 1400-1410.
5. Auffinger P, Westhof E. 1999. Singly and bifurcated hydrogen-bonded base-pairs in tRNA anticodon hairpins and ribozymes. J Mol Biol 292: 467-483.
6. Ser. Science 263: 1404-1410.
7. Bjork GR, Jacobsson K, Nilsson K, Johansson MJ, Bystrom AS, Persson OP. 2001. A primordial tRNA modification required for the evolution of life? EMBO J 20: 231-239.
8. 2U) in lysyl-tRNA is required for viability in yeast. RNA 13: 1245-1255.
9. Chen C, Huang B, Eliasson M, Ryden P, Bystrom AS. 2011. Elongator complex influences telomeric gene silencing and DNA damage response by its role in wobble uridine tRNA modification. PLoS Genet 7: e1002258.
10. Dihanich ME, Najarian D, Clark R, Gillman EC, Martin NC, Hopper AK. 1987. Isolation and characterization of MOD5, a gene required for isopentenylation of cytoplasmic and mitochondrial tRNAs of Saccharomyces cerevisiae. Mol Cell Biol 7: 177-184.
11. D'Silva S, Haider SJ, Phizicky EM. 2011. A domain of the actin binding protein Abp140 is the yeast methyltransferase responsible for 3-methylcytidine modification in the tRNA anti-codon loop. RNA 17: 1100-1110.
12. El Yacoubi B, Lyons B, Cruz Y, Reddy R, Nordin B, Agnelli F, Williamson JR, Schimmel P, Swairjo MA, de Crecy-Lagard V. 2009. The universal YrdC/Sua5 family is required for the formation of threonylcarbamoyladenosine in tRNA. Nucleic Acids Res 37: 2894-2909.
13. El Yacoubi B, Hatin I, Deutsch C, Kahveci T, Rousset JP, Iwata-Reuyl D, Murzin AG, de Crécy-Lagard V. 2011. A role for the universal Kae1/Qri7/YgjD (COG0533) family in tRNA modification. EMBO J 30: 882-893.
14. Esberg A, Huang B, Johansson MJ, Bystrom AS. 2006. Elevated levels of two tRNA species bypass the requirement for elongator complex in transcription and exocytosis. Mol Cell 24: 139-148.
15. Fleming IM, Paris Z, Gaston KW, Balakrishnan R, Fredrick K, Rubio MA, Alfonzo JD. 2016. A tRNA methyltransferase paralog is important for ribosome stability and cell division in Trypanosoma brucei. Sci Rep 6: 21438.
16. Gelperin DM, White MA, Wilkinson ML, Kon Y, Kung LA, Wise KJ, Lopez-Hoyo N, Jiang L, Piccirillo S, Yu H, et al. 2005. Biochemical and genetic analysis of the yeast proteome with a movable ORF collection. Genes Dev 19: 2816-2826.
17. Gerber AP, Keller W. 1999. An adenosine deaminase that generates ino-sine at the wobble position of tRNAs. Science 286: 1146-1149.
18. Grant TD, Snell EH, Luft JR, Quartley E, Corretore S, Wolfley JR, Snell ME, Hadd A, Perona JJ, Phizicky EM, et al. 2012. Structural conservation of an ancient tRNA sensor in eukaryotic glutaminyl-tRNA synthetase. Nucleic Acids Res 40: 3723-3731.
19. Guo M, Yang XL, Schimmel P. 2010. New functions of aminoacyl-tRNA synthetases beyond translation. Nat Rev Mol Cell Biol 11: 668-674.
20. Guy MP, Phizicky EM. 2014. Two-subunit enzymes involved in eukaryotic post-transcriptional tRNA modification. RNA Biol 11: 1608-1618.
21. Phe anticodon loop in eukaryotes. RNA 21: 61-74.
22. Phe anti-codon loop. RNA 18: 1921-1933.
23. Guy MP, Young DL, Payea MJ, Zhang X, Kon Y, Dean KM, Grayhack EJ, Mathews DH, Fields S, Phizicky EM. 2014. Identification of the determinants of tRNA function and susceptibility to rapid tRNA decay by high-throughput in vivo analysis. Genes Dev 28: 1721-1732.
24. ′-O-methylation are implicated in nonsyndromic X-linked intellectual disability due to mutations in FTSJ1. Hum Mutat 36: 1176-1187.
25. Hall TM. 2005. Multiple modes of RNA recognition by zinc finger pro-teins. Curr Opin Struct Biol 15: 367-373.
26. 2U modification in yeast. RNA 21: 188-201.
27. Lys. Biochemistry 38: 13338-13346.
28. Herbert CJ, Labouesse M, Dujardin G, Slonimski PP. 1988. The NAM2 proteins from S. cerevisiae and S. douglasii are mitochondrial leucyl-tRNA synthetases, and are involved in mRNA splicing. EMBO J 7: 473-483.
29. Leu in vitro. J Mol Biol 268: 704-711.
30. Hur S, Stroud RM. 2007. How U38, 39, and 40 of many tRNAs become the targets for pseudouridylation by TruA. Mol Cell 26: 189-203.
31. His by recognition of the anticodon, one of several features unexpectedly shared with tRNA synthetases. RNA 12: 1007-1014.
32. 1G methyltransferase responsible for modification at position 9. RNA 9: 574-585.
33. Janke C, Magiera MM, Rathfelder N, Taxis C, Reber S, Maekawa H, Moreno-Borchart A, Doenges G, Schwob E, Schiebel E, et al. 2004. A versatile toolbox for PCR-based tagging of yeast genes: new fluorescent proteins, more markers and promoter substitution cassettes. Yeast 21: 947-962.
34. 4-acetylcytidine formation in tRNA. RNA 10: 712-719.
35. Johansson MJ, Esberg A, Huang B, Bjork GR, Bystrom AS. 2008. Eukaryotic wobble uridine modifications promote a functionally redundant decoding system. Mol Cell Biol 28: 3301-3312.
36. Juhling F, Morl M, Hartmann RK, Sprinzl M, Stadler PF, Putz J. 2009. tRNAdb 2009: compilation of tRNA sequences and tRNA genes. Nucleic Acids Res 37: D159-D162.
37. Met in S. cerevisiae. Genes Dev 18: 1227-1240.
38. GGC to ensure accurate decoding. Nat Struct Mol Biol 16: 359-364.
39. Lu D, Searles MA, Klug A. 2003. Crystal structure of a zinc-finger-RNA complex reveals two modes of molecular recognition. Nature 426: 96-100.
40. Lustig F, Boren T, Claesson C, Simonsson C, Barciszewska M, Lagerkvist U. 1993. The nucleotide in position 32 of the tRNA anti-codon loop determines ability of anticodon UCC to discriminate among glycine codons. Proc Natl Acad Sci 90: 3343-3347.
41. Macbeth MR, Schubert HL, Vandemark AP, Lingam AT, Hill CP, Bass BL. 2005. Inositol hexakisphosphate is bound in the ADAR2 core and required for RNA editing. Science 309: 1534-1539.
42. Machnicka MA, Milanowska K, Osman Oglou O, Purta E, Kurkowska M, Olchowik A, Januszewski W, Kalinowski S, Dunin-Horkawicz S, Rother KM, et al. 2013. MODOMICS: a database of RNA modification pathways-2013 update. Nucleic Acids Res 41: D262-D267.
43. 6-threonylcar-bamoyladenosine as a widely distributed tRNA hypermodification. Nat Chem Biol 9: 105-111.
44. Moitoso de Vargas L, Pargellis CA, Hasan NM, Bushman EW, Landy A. 1988. Autonomous DNA binding domains of a; integrase recognize two different sequence families. Cell 54: 923-929.
45. Murphy FVt, Ramakrishnan V. 2004. Structure of a purine-purine wobble base pair in the decoding center of the ribosome. Nat Struct Mol Biol 11: 1251-1252.
46. Na JG, Pinto I, Hampsey M. 1992. Isolation and characterization of SUA5, a novel gene required for normal growth in Saccharomyces cerevisiae. Genetics 131: 791-801.
47. Nakamura A, Nemoto T, Heinemann IU, Yamashita K, Sonoda T, Komoda K, Tanaka I, Soll D, Yao M. 2013. Structural basis of reverse nucleotide polymerization. Proc Natl Acad Sci 110: 20970-20975.
48. Nolte RT, Conlin RM, Harrison SC, Brown RS. 1998. Differing roles for zinc fingers in DNA recognition: structure of a six-finger transcription factor IIIA complex. Proc Natl Acad Sci 95: 2938-2943.
49. Noma A, Yi S, Katoh T, Takai Y, Suzuki T, Suzuki T. 2011. Actin-bind-ing protein ABP140 is a methyltransferase for 3-methylcytidine at position 32 of tRNAs in Saccharomyces cerevisiae. RNA 17: 1111-1119.
50. Olejniczak M, Uhlenbeck OC. 2006. tRNA residues that have coevolved with their anticodon to ensure uniform and accurate codon recogni-tion. Biochimie 88: 943-950.
51. Olejniczak M, Dale T, Fahlman RP, Uhlenbeck OC. 2005. Idiosyncratic tuning of tRNAs to achieve uniform ribosome binding. Nat Struct Mol Biol 12: 788-793.
52. ′-O-methylriboses in yeast tRNA anticodon loop. EMBO J 21: 1811-1820.
53. Quartley E, Alexandrov A, Mikucki M, Buckner FS, Hol WG, DeTitta GT, Phizicky EM, Grayhack EJ. 2009. Heterologous expression of L. major proteins in S. cerevisiae: a test of solubility, purity, and gene recoding. J Struct Funct Genomics 10: 233-247.
54. Sampath P, Mazumder B, Seshadri V, Gerber CA, Chavatte L, Kinter M, Ting SM, Dignam JD, Kim S, Driscoll DM, et al. 2004. Noncanonical function of glutamyl-prolyl-tRNA synthetase: gene-specific silencing of translation. Cell 119: 195-208.
55. Sarkar J, Poruri K, Boniecki MT, McTavish KK, Martinis SA. 2012. Yeast mitochondrial leucyl-tRNA synthetase CP1 domain has functionally diverged to accommodate RNA splicing at expense of hydrolytic editing. J Biol Chem 287: 14772-14781.
56. Sharma S, Langhendries JL, Watzinger P, Kotter P, Entian KD, Lafontaine DL. 2015. Yeast Kre33 and human NAT10 are conserved 18S rRNA cytosine acetyltransferases that modify tRNAs assisted by the adaptor Tan1/THUMPD1. Nucleic Acids Res 43: 2242-2258.
57. Shimada N, Suzuki T, Watanabe K. 2001. Dual mode recognition of two isoacceptor tRNAs by mammalian mitochondrial seryl-tRNA syn-thetase. J Biol Chem 276: 46770-46778.
58. Smirnova EV, Lakunina VA, Tarassov I, Krasheninnikov IA, Kamenski PA. 2012. Noncanonical functions of aminoacyl-tRNA synthetases. Biochemistry (Mosc) 77: 15-25.
59. Swinehart WE, Jackman JE. 2015. Diversity in mechanism and function of tRNA methyltransferases. RNA Biol 12: 398-411.
60. 1G9 methyltrans-ferase Trm10. RNA 19: 1137-1146.
61. Urbonavicius J, Qian Q, Durand JM, Hagervall TG, Bjork GR. 2001. Improvement of reading frame maintenance is a common function for several tRNA modifications. EMBO J 20: 4863-4873.
62. Waas WF, Druzina Z, Hanan M, Schimmel P. 2007. Role of a tRNA base modification and its precursors in frameshifting in eukaryotes. J Biol Chem 282: 26026-26034.
63. Wakasugi K, Schimmel P. 1999. Two distinct cytokines released from a human aminoacyl-tRNA synthetase. Science 284: 147-151.
64. Sec complex structures reveal mechanism of the first step in selenocysteine biosynthesis. Nucleic Acids Res 43: 10534-10545.
65. Weissenbach J, Kiraly I, Dirheimer G. 1977. Primary structure of tRNA Thr 1a and b from brewer's yeast. Biochimie 59: 381-391.
66. Weixlbaumer A, Murphy FVt, Dziergowska A, Malkiewicz A, Vendeix FA, Agris PF, Ramakrishnan V. 2007. Mechanism for expanding the decoding capacity of transfer RNAs by modification of uridines. Nat Struct Mol Biol 14: 498-502.
67. Whipple JM, Lane EA, Chernyakov I, D'Silva S, Phizicky EM. 2011. The yeast rapid tRNA decay pathway primarily monitors the structural integrity of the acceptor and T-stems of mature tRNA. Genes Dev 25: 1173-1184.
68. Yao P, Fox PL. 2013. Aminoacyl-tRNA synthetases in medicine and disease. EMBO Mol Med 5: 332-343.