2,489
Views
38
CrossRef citations to date
0
Altmetric
Research Paper

TRMT2B is responsible for both tRNA and rRNA m5U-methylation in human mitochondria

&
Pages 451-462 | Received 07 Oct 2019, Accepted 02 Jan 2020, Published online: 17 Jan 2020

References

  • Rebelo-Guiomar P, Powell CA, Van Haute L, et al. The mammalian mitochondrial epitranscriptome. Biochim Biophys Acta - Gene Regul Mech. 2019;1862(3):429–446.
  • Van Haute L, Dietmann S, Kremer L, et al. Deficient methylation and formylation of mt-tRNAMet wobble cytosine in a patient carrying mutations in NSUN3. Nat Commun. 2016;7:12039.
  • Garone C, D’Souza AR, Dallabona C, et al. Defective mitochondrial rRNA methyltransferase MRM2 causes MELAS-like clinical syndrome. Hum Mol Genet. 2017;26(21):4257–4266.
  • Powell CA, Nicholls TJ, Minczuk M. Nuclear-encoded factors involved in post-transcriptional processing and modification of mitochondrial tRNAs in human disease. Front Genet. 2015;6:79.
  • Boczonadi V, Ricci G, Horvath R. Mitochondrial DNA transcription and translation: clinical syndromes. Essays Biochem. 2018;62(3):321–340.
  • Bessho Y, Shibata R, Sekine SI, et al. Structural basis for functional mimicry of long-variable-arm tRNA by transfer-messenger RNA. Proc Natl Acad Sci. 2007;104(20):8293–8298.
  • Kazantsev AV, Krivenko AA, Harrington DJ, et al. Crystal structure of a bacterial ribonuclease P RNA. Proc Natl Acad Sci. 2005;102(38):13392–13397.
  • Toor N, Keating KS, Taylor SD, et al. Crystal Structure of a Self-Spliced Group II Intron. Science. 2008;320(5872):77–82.
  • Serganov A, Huang L, Patel DJ. Coenzyme recognition and gene regulation by a flavin mononucleotide riboswitch. Nature. 2009;458(7235):233–237.
  • Chan CW, Chetnani B, Mondragón A. Structure and function of the T-loop structural motif in noncoding RNAs. Wiley Interdiscip Rev RNA. 2013;4(5):507–522.
  • Dubin DT. Methylated nucleotide content of mitochondrial ribosomal RNA from hamster cells. J Mol Biol. 1974;84(2):257–273.
  • Baer RJ, Dubin DT. Methylated regions of hamster mitochondrial ribosomal RNA: structural and functional correlates. Nucleic Acids Res. 1981;9(2):323–337.
  • Madsen CT, Mengel-Jørgensen J, Kirpekar F, et al. Identifying the methyltransferases for m(5)U747 and m(5)U1939 in 23S rRNA using MALDI mass spectrometry. Nucleic Acids Res. 2003;31(16):4738–4746.
  • Ranaei-Siadat E, Fabret C, Seijo B, et al. RNA-methyltransferase TrmA is a dual-specific enzyme responsible for C5-methylation of uridine in both tmRNA and tRNA. RNA Biol. 2013;10(4):572–578.
  • Gu X, Ofengand J, Santi DV. In vitro methylation of Escherichia coli 16S rRNA by tRNA (m5U54)-methyltransferase. Biochemistry. 1994;33(8):2255–2261.
  • Alian A, Lee TT, Griner SL, et al. Structure of a TrmA-RNA complex: A consensus RNA fold contributes to substrate selectivity and catalysis in m5U methyltransferases. Proc Natl Acad Sci U S A. 2008;105(19):6876–6881.
  • Bjork GR, Neidhardt FC. Physiological and Biochemical Studies on the Function of 5-Methyluridine in the Transfer Ribonucleic Acid of Escherichia coli. J Bacteriol. 1975;124(1):99–111.
  • Persson BC, Gustafsson C, Bergt DE, et al. The gene for a tRNA modifying enzyme, m5U54-methyltransferase, is essential for viability in Escherichia coli. Biochemistry. 1992;89:3995–3998.
  • Hopper AK, Furukawa AH, Pham HD, et al. Defects in modification of cytoplasmic and mitochondrial transfer RNAs are caused by single nuclear mutations. Cell. 1982;28(3):543–550.
  • Nordlund ME, Johansson JO, von Pawel-rammingen U, et al. Identification of the TRM2 gene encoding the tRNA(m5U54)methyltransferase of Saccharomyces cerevisiae. RNA. 2000;6(6):844–860.
  • Johansson MJO, Byström AS. Dual function of the tRNA(m(5)U54)methyltransferase in tRNA maturation. RNA. 2002;8(3):324–335.
  • Choudhury SA, Asefa B, Webb A, et al. Functional and genetic analysis of the Saccharomyces cerevisiae RNC1/TRM2: evidences for its involvement in DNA double-strand break repair. Mol Cell Biochem. 2007;300(1–2):215–226.
  • Carter J-M, Emmett W, Mozos IR, et al. FICC-Seq: a method for enzyme-specified profiling of methyl-5-uridine in cellular RNA. Nucleic Acids Res. 2019;47(19):113.
  • De Crécy-Lagard V, Boccaletto P, Mangleburg CG, et al. Matching tRNA modifications in humans to their known and predicted enzymes. Nucleic Acids Res. 2019;47(5):2143–2159.
  • Machnicka MA, Milanowska K, Osman Oglou O, et al. MODOMICS: a database of RNA modification pathways–2013 update. Nucleic Acids Res. 2013;41(D1):D262–D267.
  • Suzuki T, Suzuki T. A complete landscape of post-transcriptional modifications in mammalian mitochondrial tRNAs. Nucleic Acids Res. 2014;42(11):7346–7357.
  • Claros MG, Vincens P. Computational method to predict mitochondrially imported proteins and their targeting sequences. Eur J Biochem. 1996;241(3):779–786.
  • Emanuelsson O, Nielsen H, Brunak S, et al. Predicting Subcellular Localization of Proteins Based on their N-terminal Amino Acid Sequence. J Mol Biol. 2000;300(4):1005–1016.
  • Small I, Peeters N, Legeai F, et al. A tool for rapidly screening proteomes for N-terminal targeting sequences. Proteomics. 2004;4(6):1581–1590.
  • Brulé H, Holmes WM, Keith G, et al. Effect of a mutation in the anticodon of human mitochondrial tRNA Pro on its post-transcriptional modification pattern. Nucleic Acids Res. 1998;26(2):537–543.
  • Desai PM, Culver GM, Rife JP. Site-directed mutants of 16S rRNA reveal important RNA domains for KsgA function and 30S subunit assembly. Biochemistry. 2011;50(5):854–863.
  • Degoul F, Brulé H, Cepanec C, et al. Isoleucylation properties of native human mitochondrial tRNAIle and tRNAIle transcripts. Implications for cardiomyopathy-related point mutations (4269, 4317) in the tRNAIle gene. Hum Mol Genet. 1998;7(3):347–354.
  • Helm M, Giegé R, Florentz C. A Watson−Crick Base-Pair-Disrupting Methyl Group (m1A9) Is Sufficient for Cloverleaf Folding of Human Mitochondrial tRNA Lys. Biochemistry. 1999;38(40):13338–13346.
  • Toompuu M, Yasukawa T, Suzuki T, et al. The 7472insC mitochondrial DNA mutation impairs the synthesis and extent of aminoacylation of tRNASer(UCN) but not its structure or rate of turnover. J Biol Chem. 2002;277(25):22240–22250.
  • Pütz J, Dupuis B, Sissler M, et al. Mamit-tRNA, a database of mammalian mitochondrial tRNA primary and secondary structures. RNA. 2007;13(8):1184–1190.
  • Hegg LA, Thurlow DL. Residual tRNA secondary structure in “denaturing” 8M urea/TBE polyacrylamide gels: effects on electrophoretic mobility and dependency on prior chemical modification of the tRNA. Nucleic Acids Res. 1990;18(10):2993–3000.
  • Davanloo P, Sprinzl M, Watanabet K, et al. Role of ribothymidine in the thermal stability of transfer RNA as monitored by proton magnetic resonance. Nucleic Acids Res. 1979;6(4April).
  • Okamoto M, Fujiwara M, Hori M, et al. tRNA Modifying Enzymes, NSUN2 and METTL1, Determine Sensitivity to 5-Fluorouracil in HeLa Cells. 2014;10(9):e1004639.
  • Knight E. Mitochondria-associated ribonucleic acid of the HeLa cell. Effect of ethidium bromide on the synthesis of ribosomal and 4S ribonucleic acid. Biochemistry. 1969;8(12):5089–5093.
  • Yasukawa T, Hino N, Suzuki T, et al. A pathogenic point mutation reduces stability of mitochondrial mutant tRNA(Ile). Nucleic Acids Res. 2000;28(19):3779–3784.
  • Metodiev MD, Lesko N, Park CB, et al. Methylation of 12S rRNA Is Necessary for In Vivo Stability of the Small Subunit of the Mammalian Mitochondrial Ribosome. Cell Metab. 2009;9(4):386–397.
  • Bar-Yaacov D, Frumkin I, Yashiro Y, et al. Mitochondrial 16S rRNA Is Methylated by tRNA Methyltransferase TRMT61B in All Vertebrates. PLoS Biol. 2016;14(9):e1002557.
  • Auxilien S, Rasmussen A, Rose S, et al. Specificity shifts in the rRNA and tRNA nucleotide targets of archaeal and bacterial m5U methyltransferases. RNA. 2011;17(1):45–53.
  • Laptev I, Shvetsova E, Levitskii S, et al. Mouse Trmt2B protein is a dual specific mitochondrial metyltransferase responsible for m 5 U formation in both tRNA and rRNA. RNA Biol. 2019 November;1–10.
  • Pang H, Ihara M, Kuchino Y, et al. Structure of a modified nucleoside in archaebacterial tRNA which replaces ribosylthymine. 1-Methylpseudouridine. J Biol Chem. 1982;257(7):3589–3592.
  • Zamir A, Holley RW, Marquisee M. Evidence for the occurence of a common pentanucleotide sequence in the structures of transfer ribonucleic acids. J Biol Chem. 1965;240:1267–1273.
  • Salinas-Giegé T, Giegé R, Giegé P. tRNA Biology in Mitochondria. Int J Mol Sci. 2015;16(3):4518–4559.
  • Van HL, Hendrick AG, D’Souza AR, et al. METTL15 introduces N4-methylcytidine into human mitochondrial 12S rRNA and is required for mitoribosome biogenesis. Nucleic Acids Res. 2019;47(19):10267–10281.
  • Metodiev MD, Spåhr H, Loguercio Polosa P, et al., ed. NSUN4 Is a Dual Function Mitochondrial Protein Required for Both Methylation of 12S rRNA and Coordination of Mitoribosomal Assembly. Barsh GS. PLoS Genet. 2014;10(2):e1004110
  • Seidel-Rogol BL, McCulloch V, Shadel GS. Human mitochondrial transcription factor B1 methylates ribosomal RNA at a conserved stem-loop. Nat Genet. 2003;33(1):23–24.
  • Rorbach J, Boesch P, Gammage PA, et al. MRM2 and MRM3 are involved in biogenesis of the large subunit of the mitochondrial ribosome. Mol Biol Cell. 2014;25(17):2542–2555.
  • Zaganelli S, Rebelo-Guiomar P, Maundrell K, et al. The pseudouridine synthase RPUSD4 is an essential component of mitochondrial RNA granules. J Biol Chem. 2017;292(11):4519–4532.
  • Minczuk M, Kolasinska-Zwierz P, Murphy MP, et al. Construction and testing of engineered zinc-finger proteins for sequence-specific modification of mtDNA. Nat Protoc. 2010;5(2):342–356.
  • Rorbach J, Gao F, Powell CA, et al. Human mitochondrial ribosomes can switch their structural RNA composition. Proc Natl Acad Sci. 2016;113(43):12198–12201.
  • Pearce SF, Rorbach J, Van Haute L, et al. Maturation of selected human mitochondrial tRNAs requires deadenylation. Elife. 2017; 6.