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PMID: 28230814 Published · epublish English Journal Article Review Research Support, Non-U.S. Gov't

m1A Post-Transcriptional Modification in tRNAs.

Biomolecules ·Vol. 7 ·No. 1 ·2017-00-21

Oerum S, Dégut C, Barraud P, Tisné C

Abstract

To date, about 90 post-transcriptional modifications have been reported in tRNA expanding their chemical and functional diversity. Methylation is the most frequent post-transcriptional tRNA modification that can occur on almost all nitrogen sites of the nucleobases, on the C5 atom of pyrimidines, on the C2 and C8 atoms of adenosine and, additionally, on the oxygen of the ribose 2'-OH. The methylation on the N1 atom of adenosine to form 1-methyladenosine (m1A) has been identified at nucleotide position 9, 14, 22, 57, and 58 in different tRNAs. In some cases, these modifications have been shown to increase tRNA structural stability and induce correct tRNA folding. This review provides an overview of the currently known m1A modifications, the different m1A modification sites, the biological role of each modification, and the enzyme responsible for each methylation in different species. The review further describes, in detail, two enzyme families responsible for formation of m1A at nucleotide position 9 and 58 in tRNA with a focus on the tRNA binding, m1A mechanism, protein domain organisation and overall structures.

Keywords
1-methyladenosine Trm10 Trm6–Trm61 TrmI Trmt10C m1A tRNA methylation
MeSH Terms
Adenosine/analogs & derivatives,metabolism Animals Enzymes/metabolism Humans Methylation Models, Molecular RNA Processing, Post-Transcriptional RNA, Transfer/chemistry,genetics,metabolism
Chemicals
Enzymes 1-methyladenosine RNA, Transfer Adenosine
Authors & Affiliations
4 authors, click to expand affiliations / ORCID
Oerum Stephanie
Institut de Biologie Physico-chimique (IBPC), CNRS, UMR 8261 CNRS/Université Paris Diderot, 13 rue Pierre et Marie Curie, Paris 75005, France. oerum@ibpc.fr.
Dégut Clément
Institut de Biologie Physico-chimique (IBPC), CNRS, UMR 8261 CNRS/Université Paris Diderot, 13 rue Pierre et Marie Curie, Paris 75005, France. c.degut@gmail.com.
Barraud Pierre
Institut de Biologie Physico-chimique (IBPC), CNRS, UMR 8261 CNRS/Université Paris Diderot, 13 rue Pierre et Marie Curie, Paris 75005, France. pierre.barraud@cnrs.fr.
Tisné Carine
Institut de Biologie Physico-chimique (IBPC), CNRS, UMR 8261 CNRS/Université Paris Diderot, 13 rue Pierre et Marie Curie, Paris 75005, France. carine.tisne@cnrs.fr.
References (92)
92 references, click to expand
  1. A novel enzymatic pathway leading to 1-methylinosine modification in Haloferax volcanii tRNA.
    Nucleic Acids Res. 1995 Nov 11;23(21):4312-9 PMID: 7501451
  2. Impact of disease-related mitochondrial mutations on tRNA structure and function.
    Trends Biochem Sci. 2003 Nov;28(11):605-11 PMID: 14607091
  3. Nuclear surveillance and degradation of hypomodified initiator tRNAMet in S. cerevisiae.
    Genes Dev. 2004 Jun 1;18(11):1227-40 PMID: 15145828
  4. RNA nucleotide methylation.
    Wiley Interdiscip Rev RNA. 2011 Sep-Oct;2(5):611-31 PMID: 21823225
  5. A primordial RNA modification enzyme: the case of tRNA (m1A) methyltransferase.
    Nucleic Acids Res. 2004 Jan 22;32(2):465-76 PMID: 14739239
  6. Grouping together highly diverged PD-(D/E)XK nucleases and identification of novel superfamily members using structure-guided alignment of sequence profiles.
    J Mol Microbiol Biotechnol. 2001 Jan;3(1):69-72 PMID: 11200231
  7. Mamit-tRNA, a database of mammalian mitochondrial tRNA primary and secondary structures.
    RNA. 2007 Aug;13(8):1184-90 PMID: 17585048
  8. Recessive Mutations in TRMT10C Cause Defects in Mitochondrial RNA Processing and Multiple Respiratory Chain Deficiencies.
    Am J Hum Genet. 2016 May 5;98 (5):993-1000 PMID: 27132592
  9. tRNA methyltransferase homolog gene TRMT10A mutation in young onset diabetes and primary microcephaly in humans.
    PLoS Genet. 2013 Oct;9(10):e1003888 PMID: 24204302
  10. Trmt61B is a methyltransferase responsible for 1-methyladenosine at position 58 of human mitochondrial tRNAs.
    RNA. 2012 Dec;18(12):2269-76 PMID: 23097428
  11. Complexes of tRNA and maturation enzymes: shaping up for translation.
    Curr Opin Struct Biol. 2007 Jun;17(3):293-301 PMID: 17580114
  12. Roles of conserved amino acid sequence motifs in the SpoU (TrmH) RNA methyltransferase family.
    J Biol Chem. 2005 Mar 18;280(11):10368-77 PMID: 15637073
  13. Primary structure of Bacillus subtilis tRNAsTyr.
    Biochem Biophys Res Commun. 1980 Jul 16;95(1):461-7 PMID: 6158319
  14. Heat-induced stability of tRNA from an extreme thermophile, Thermus thermophilus.
    Biochem Biophys Res Commun. 1976 Oct 4;72(3):1137-44 PMID: 985514
  15. The essential Gcd10p-Gcd14p nuclear complex is required for 1-methyladenosine modification and maturation of initiator methionyl-tRNA.
    Genes Dev. 1998 Dec 1;12(23):3650-62 PMID: 9851972
  16. Transcriptome-wide mapping reveals reversible and dynamic N(1)-methyladenosine methylome.
    Nat Chem Biol. 2016 May;12 (5):311-6 PMID: 26863410
  17. A divalent metal ion-dependent N(1)-methyl transfer to G37-tRNA.
    Chem Biol. 2014 Oct 23;21(10):1351-60 PMID: 25219964
  18. A Watson-Crick base-pair-disrupting methyl group (m1A9) is sufficient for cloverleaf folding of human mitochondrial tRNALys.
    Biochemistry. 1999 Oct 5;38(40):13338-46 PMID: 10529209
  19. The tRNA recognition mechanism of the minimalist SPOUT methyltransferase, TrmL.
    Nucleic Acids Res. 2013 Sep;41(16):7828-42 PMID: 23804755
  20. Short-chain dehydrogenases/reductases (SDR).
    Biochemistry. 1995 May 9;34(18):6003-13 PMID: 7742302
  21. Cloning and characterization of tRNA (m1A58) methyltransferase (TrmI) from Thermus thermophilus HB27, a protein required for cell growth at extreme temperatures.
    Nucleic Acids Res. 2003 Apr 15;31(8):2148-56 PMID: 12682365
  22. Short-chain dehydrogenase/reductase (SDR) relationships: a large family with eight clusters common to human, animal, and plant genomes.
    Protein Sci. 2002 Mar;11(3):636-41 PMID: 11847285
  23. Structural and evolutionary bioinformatics of the SPOUT superfamily of methyltransferases.
    BMC Bioinformatics. 2007 Mar 05;8:73 PMID: 17338813
  24. Crystal structure of Rv2118c: an AdoMet-dependent methyltransferase from Mycobacterium tuberculosis H37Rv.
    J Mol Biol. 2001 Sep 14;312(2):381-91 PMID: 11554794
  25. Crystal Structure of the Human tRNA m(1)A58 Methyltransferase-tRNA(3)(Lys) Complex: Refolding of Substrate tRNA Allows Access to the Methylation Target.
    J Mol Biol. 2015 Dec 4;427(24):3862-76 PMID: 26470919
  26. Medium- and short-chain dehydrogenase/reductase gene and protein families : the SDR superfamily: functional and structural diversity within a family of metabolic and regulatory enzymes.
    Cell Mol Life Sci. 2008 Dec;65(24):3895-906 PMID: 19011750
  27. tRNAdb 2009: compilation of tRNA sequences and tRNA genes.
    Nucleic Acids Res. 2009 Jan;37(Database issue):D159-62 PMID: 18957446
  28. Reversal of DNA alkylation damage by two human dioxygenases.
    Proc Natl Acad Sci U S A. 2002 Dec 24;99(26):16660-5 PMID: 12486230
  29. Modification defect at anticodon wobble nucleotide of mitochondrial tRNAs(Leu)(UUR) with pathogenic mutations of mitochondrial myopathy, encephalopathy, lactic acidosis, and stroke-like episodes.
    J Biol Chem. 2000 Feb 11;275(6):4251-7 PMID: 10660592
  30. Insights into catalysis by a knotted TrmD tRNA methyltransferase.
    J Mol Biol. 2003 Nov 7;333(5):931-49 PMID: 14583191
  31. Towards understanding human mitochondrial leucine aminoacylation identity.
    J Mol Biol. 2003 May 16;328(5):995-1010 PMID: 12729737
  32. ALKBH1-Mediated tRNA Demethylation Regulates Translation.
    Cell. 2016 Oct 20;167(3):816-828.e16 PMID: 27745969
  33. Structural and functional insights into tRNA binding and adenosine N1-methylation by an archaeal Trm10 homologue.
    Nucleic Acids Res. 2016 Jan 29;44(2):940-53 PMID: 26673726
  34. Mechanism of N-methylation by the tRNA m1G37 methyltransferase Trm5.
    RNA. 2010 Dec;16(12):2484-92 PMID: 20980671
  35. Distribution and frequencies of post-transcriptional modifications in tRNAs.
    RNA Biol. 2014;11(12):1619-29 PMID: 25611331
  36. The crystal structure of the zinc phosphodiesterase from Escherichia coli provides insight into function and cooperativity of tRNase Z-family proteins.
    J Bacteriol. 2006 Feb;188(4):1607-14 PMID: 16452444
  37. Tertiary structure checkpoint at anticodon loop modification in tRNA functional maturation.
    Nat Struct Mol Biol. 2009 Oct;16(10):1109-15 PMID: 19749755
  38. Identification of two tRNA thiolation genes required for cell growth at extremely high temperatures.
    J Biol Chem. 2006 May 19;281(20):14296-306 PMID: 16547008
  39. Enzymatic conversion of adenosine to inosine and to N1-methylinosine in transfer RNAs: a review.
    Biochimie. 1996;78(6):488-501 PMID: 8915538
  40. Many paths to methyltransfer: a chronicle of convergence.
    Trends Biochem Sci. 2003 Jun;28(6):329-35 PMID: 12826405
  41. tRNA stabilization by modified nucleotides.
    Biochemistry. 2010 Jun 22;49(24):4934-44 PMID: 20459084
  42. RNase P without RNA: identification and functional reconstitution of the human mitochondrial tRNA processing enzyme.
    Cell. 2008 Oct 31;135(3):462-74 PMID: 18984158
  43. Crystal structure of the two-subunit tRNA m(1)A58 methyltransferase TRM6-TRM61 from Saccharomyces cerevisiae.
    Sci Rep. 2016 Sep 01;6:32562 PMID: 27582183
  44. The 3 A crystal structure of yeast initiator tRNA: functional implications in initiator/elongator discrimination.
    EMBO J. 1991 Oct;10(10):3105-11 PMID: 1915284
  45. Two tRNAIle1 species from an extreme thermophile, Thermus thermophilus HB8: effect of 2-thiolation of ribothymidine on the thermostability of tRNA.
    Biochemistry. 1985 Oct 8;24(21):5711-5 PMID: 3853464
  46. In silico analysis of the tRNA:m1A58 methyltransferase family: homology-based fold prediction and identification of new members from Eubacteria and Archaea.
    FEBS Lett. 2001 Oct 26;507(2):123-7 PMID: 11684083
  47. tRNA transfers to the limelight.
    Genes Dev. 2003 Jan 15;17(2):162-80 PMID: 12533506
  48. Structural basis for methyl-donor-dependent and sequence-specific binding to tRNA substrates by knotted methyltransferase TrmD.
    Proc Natl Acad Sci U S A. 2015 Aug 4;112(31):E4197-205 PMID: 26183229
  49. Crystal structure of tRNA(m1G37)methyltransferase: insights into tRNA recognition.
    EMBO J. 2003 Jun 2;22(11):2593-603 PMID: 12773376
  50. The dynamic N(1)-methyladenosine methylome in eukaryotic messenger RNA.
    Nature. 2016 Feb 25;530(7591):441-6 PMID: 26863196
  51. mRNA modifications: Dynamic regulators of gene expression?
    RNA Biol. 2016 Sep;13(9):760-5 PMID: 27351916
  52. The m1A(58) modification in eubacterial tRNA: An overview of tRNA recognition and mechanism of catalysis by TrmI.
    Biophys Chem. 2016 Mar;210:27-34 PMID: 26189113
  53. Methylated nucleosides in tRNA and tRNA methyltransferases.
    Front Genet. 2014 May 23;5:144 PMID: 24904644
  54. The bipartite structure of the tRNA m1A58 methyltransferase from S. cerevisiae is conserved in humans.
    RNA. 2005 Aug;11(8):1281-90 PMID: 16043508
  55. Control of catalytic cycle by a pair of analogous tRNA modification enzymes.
    J Mol Biol. 2010 Jul 9;400(2):204-17 PMID: 20452364
  56. Identification of 113 conserved essential genes using a high-throughput gene disruption system in Streptococcus pneumoniae.
    Nucleic Acids Res. 2002 Jul 15;30(14):3152-62 PMID: 12136097
  57. Insights into the hyperthermostability and unusual region-specificity of archaeal Pyrococcus abyssi tRNA m1A57/58 methyltransferase.
    Nucleic Acids Res. 2010 Oct;38(18):6206-18 PMID: 20483913
  58. The presence of modified nucleotides is required for cloverleaf folding of a human mitochondrial tRNA.
    Nucleic Acids Res. 1998 Apr 1;26(7):1636-43 PMID: 9512533
  59. Exosite modules guide substrate recognition in the ZiPD/ElaC protein family.
    J Biol Chem. 2005 May 6;280(18):17857-62 PMID: 15699034
  60. Recognition of human mitochondrial tRNALeu(UUR) by its cognate leucyl-tRNA synthetase.
    J Mol Biol. 2004 May 21;339(1):17-29 PMID: 15123417
  61. Human RNase H1 is associated with protein P32 and is involved in mitochondrial pre-rRNA processing.
    PLoS One. 2013 Aug 22;8(8):e71006 PMID: 23990920
  62. SPOUT: a class of methyltransferases that includes spoU and trmD RNA methylase superfamilies, and novel superfamilies of predicted prokaryotic RNA methylases.
    J Mol Microbiol Biotechnol. 2002 Jan;4(1):71-5 PMID: 11763972
  63. A novel cloverleaf structure found in mammalian mitochondrial tRNA(Ser) (UCN).
    Nucleic Acids Res. 1991 Nov 25;19(22):6101-5 PMID: 1840673
  64. Identification of the yeast gene encoding the tRNA m1G methyltransferase responsible for modification at position 9.
    RNA. 2003 May;9(5):574-85 PMID: 12702816
  65. New archaeal methyltransferases forming 1-methyladenosine or 1-methyladenosine and 1-methylguanosine at position 9 of tRNA.
    Nucleic Acids Res. 2010 Oct;38(19):6533-43 PMID: 20525789
  66. Methylation of an adenosine in the D-loop of specific transfer RNAs from yeast by a procaryotic tRNA (adenine-1) methyltransferase.
    Nucleic Acids Res. 1977 Jun;4(6):1769-82 PMID: 408794
  67. The Gcd10p/Gcd14p complex is the essential two-subunit tRNA(1-methyladenosine) methyltransferase of Saccharomyces cerevisiae.
    Proc Natl Acad Sci U S A. 2000 May 9;97(10):5173-8 PMID: 10779558
  68. N7-Methylguanine at position 46 (m7G46) in tRNA from Thermus thermophilus is required for cell viability at high temperatures through a tRNA modification network.
    Nucleic Acids Res. 2010 Jan;38(3):942-57 PMID: 19934251
  69. The YqfN protein of Bacillus subtilis is the tRNA: m1A22 methyltransferase (TrmK).
    Nucleic Acids Res. 2008 Jun;36(10):3252-62 PMID: 18420655
  70. tRNA recognition by a bacterial tRNA Xm32 modification enzyme from the SPOUT methyltransferase superfamily.
    Nucleic Acids Res. 2015 Sep 3;43(15):7489-503 PMID: 26202969
  71. Codon recognition patterns as deduced from sequences of the complete set of transfer RNA species in Mycoplasma capricolum. Resemblance to mitochondria.
    J Mol Biol. 1989 Sep 5;209(1):37-54 PMID: 2478713
  72. A subcomplex of human mitochondrial RNase P is a bifunctional methyltransferase--extensive moonlighting in mitochondrial tRNA biogenesis.
    Nucleic Acids Res. 2012 Dec;40(22):11583-93 PMID: 23042678
  73. Compilation of tRNA sequences and sequences of tRNA genes.
    Nucleic Acids Res. 1998 Jan 1;26(1):148-53 PMID: 9399820
  74. Human and bacterial oxidative demethylases repair alkylation damage in both RNA and DNA.
    Nature. 2003 Feb 20;421(6925):859-63 PMID: 12594517
  75. tRNA biology charges to the front.
    Genes Dev. 2010 Sep 1;24(17):1832-60 PMID: 20810645
  76. Crystal structure of Thermus thermophilus tRNA m1A58 methyltransferase and biophysical characterization of its interaction with tRNA.
    J Mol Biol. 2008 Mar 21;377(2):535-50 PMID: 18262540
  77. Nucleotide sequences of serine tRNAs from Bacillus subtilis.
    Biochim Biophys Acta. 1992 Apr 6;1130(3):333-5 PMID: 1373329
  78. Crystal structure of tRNA m1G9 methyltransferase Trm10: insight into the catalytic mechanism and recognition of tRNA substrate.
    Nucleic Acids Res. 2014 Jan;42(1):509-25 PMID: 24081582
  79. Sculpting an RNA conformational energy landscape by a methyl group modification--a single-molecule FRET study.
    Angew Chem Int Ed Engl. 2008;47(23):4326-30 PMID: 18449867
  80. TRMT10A dysfunction is associated with abnormalities in glucose homeostasis, short stature and microcephaly.
    J Med Genet. 2014 Sep;51(9):581-6 PMID: 25053765
  81. Novel predicted RNA-binding domains associated with the translation machinery.
    J Mol Evol. 1999 Mar;48(3):291-302 PMID: 10093218
  82. A methyl group controls conformational equilibrium in human mitochondrial tRNA(Lys).
    J Am Chem Soc. 2007 Nov 7;129(44):13382-3 PMID: 17941640
  83. Nuclear control of cloverleaf structure of human mitochondrial tRNA(Lys).
    J Mol Biol. 2004 Mar 26;337(3):545-60 PMID: 15019776
  84. Genome-wide analysis of N1-methyl-adenosine modification in human tRNAs.
    RNA. 2010 Jul;16(7):1317-27 PMID: 20484468
  85. Loss of the mitochondrial protein-only ribonuclease P complex causes aberrant tRNA processing and lethality in Drosophila.
    Nucleic Acids Res. 2016 Jul 27;44(13):6409-22 PMID: 27131785
  86. Role of post-transcriptional modifications of primer tRNALys,3 in the fidelity and efficacy of plus strand DNA transfer during HIV-1 reverse transcription.
    J Biol Chem. 1999 Feb 12;274(7):4412-20 PMID: 9933645
  87. RNA processing in human mitochondria.
    Cell Cycle. 2011 Sep 1;10(17):2904-16 PMID: 21857155
  88. In vitro methylation of yeast tRNAAsp by rat brain cortical tRNA-(adenine-1) methyltransferase.
    Nucleic Acids Res. 1979 Mar;6(3):1123-33 PMID: 375195
  89. THUMP--a predicted RNA-binding domain shared by 4-thiouridine, pseudouridine synthases and RNA methylases.
    Trends Biochem Sci. 2001 Apr;26(4):215-7 PMID: 11295541
  90. Crystal structure of tRNA m(1)A58 methyltransferase TrmI from Aquifex aeolicus in complex with S-adenosyl-L-methionine.
    J Struct Funct Genomics. 2014 Sep;15(3):173-80 PMID: 24894648
  91. Transfer RNA post-transcriptional processing, turnover, and subcellular dynamics in the yeast Saccharomyces cerevisiae.
    Genetics. 2013 May;194(1):43-67 PMID: 23633143
  92. Structural comparison of tRNA m(1)A58 methyltransferases revealed different molecular strategies to maintain their oligomeric architecture under extreme conditions.
    BMC Struct Biol. 2011 Dec 14;11:48 PMID: 22168821
Article Info
Journal
Biomolecules
Abbr.
Biomolecules
ISSN
2218-273X
Published
2017-00-21
Epub
2017-00-21
Language
English
Region
Switzerland
NLM ID
101596414
PMCID
PMC5372732
Subset
IM
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