CoChat
Sign Up
Cited by 517RNA modifications and cancerRNA regulation and diseaseEpigenetics and DNA Methylation

Eukaryotic 5-methylcytosine (m5C) RNA Methyltransferases: Mechanisms, Cellular Functions, and Links to Disease

Open access
Bohnsack, Katherine E., Höbartner, Claudia, Bohnsack, Markus T.·2019·Genes
DOI 10.3390/genes10020102PMC PMC6409601
Open this paper in CoChat — free accountOpen PDF

Abstract

5-methylcytosine (m5C) is an abundant RNA modification that’s presence is reported in a wide variety of RNA species, including cytoplasmic and mitochondrial ribosomal RNAs (rRNAs) and transfer RNAs (tRNAs), as well as messenger RNAs (mRNAs), enhancer RNAs (eRNAs) and a number of non-coding RNAs. In eukaryotes, C5 methylation of RNA cytosines is catalyzed by enzymes of the NOL1/NOP2/SUN domain (NSUN) family, as well as the DNA methyltransferase homologue DNMT2. In recent years, substrate RNAs and modification target nucleotides for each of these methyltransferases have been identified, and structural and biochemical analyses have provided the first insights into how each of these enzymes achieves target specificity. Functional characterizations of these proteins and the modifications they install have revealed important roles in diverse aspects of both mitochondrial and nuclear gene expression. Importantly, this knowledge has enabled a better understanding of the molecular basis of a number of diseases caused by mutations in the genes encoding m5C methyltransferases or changes in the expression level of these enzymes.

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Integrity signals

Registry

Crossref · 10.3390/genes10020102

Cites

2 of 2 references verified0 citation errors · 0 not checkable

Statistics

Claims the paper makes

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Claims other papers make about this one

Each is checked against this paper’s own text: does it say what the citing paper says it does?

Self-check

Percentages, sums and reported differences re-computed from the paper’s own numbers.

The self-check needs the paper’s full text.

Cites

Flagged first, then by citations

Research works printed but not linked: 87

  1. [1]Boccaletto P. Machnicka M.A. Purta E. Piatkowski P. Baginski B. Wirecki T.K. de Crecy-Lagard V. Ross R. Limbach P.A. Kotter A. MODOMICS: a database of RNA modification pathways. 2017 update Nucleic Acids Res. 2018 46 D303 D307 10.1093/nar/gkx1030 29106616 PMC5753262 · DOI
  2. [2]Breiling A. Lyko F. Epigenetic regulatory functions of DNA modifications: 5-methylcytosine and beyond Epigenetics Chromatin 2015 8 24 10.1186/s13072-015-0016-6 26195987 PMC4507326 · DOI
  3. [3]Trixl L. Lusser A. The dynamic RNA modification 5-methylcytosine and its emerging role as an epitranscriptomic mark Wiley Interdiscip. Rev. RNA 2019 10 e1510 10.1002/wrna.1510 30311405 PMC6492194 · DOI
  4. [4]Lyko F. The DNA methyltransferase family: a versatile toolkit for epigenetic regulation Nat. Rev. Genet. 2018 19 81 92 10.1038/nrg.2017.80 29033456 · DOI
  5. [5]Bourgeois G. Ney M. Gaspar I. Aigueperse C. Schaefer M. Kellner S. Helm M. Motorin Y. Eukaryotic rRNA modification by yeast 5- methylcytosine-methyltransferases and human proliferation-associated antigen p120 PLoS One 2015 10 1 16 10.1371/journal.pone.0133321 PMC4510066 26196125 · DOI
  6. [6]Brzezicha B. Schmidt M. Makałowska I. Jarmołowski A. Pieńkowska J. Szweykowska-Kulińska Z. Identification of human tRNA: m5C methyltransferase catalysing intron-dependent m5C formation in the first position of the anticodon of the pre-tRNA(CAA)Leu Nucleic Acids Res. 2006 34 6034 6043 10.1093/nar/gkl765 17071714 PMC1635329 · DOI
  7. [7]Blanco S. Dietmann S. Flores J.V. Hussain S. Kutter C. Humphreys P. Lukk M. Lombard P. Treps L. Popis M. Aberrant methylation of tRNAs links cellular stress to neuro-developmental disorders EMBO J. 2014 33 2020 2039 10.15252/embj.201489282 25063673 PMC4195770 · DOI
  8. [8]Tuorto F. Liebers R. Musch T. Schaefer M. Hofmann S. Kellner S. Frye M. Helm M. Stoecklin G. Lyko F. RNA cytosine methylation by Dnmt2 and NSun2 promotes tRNA stability and protein synthesis Nat. Struct. Mol. Biol. 2012 19 900 905 10.1038/nsmb.2357 22885326 · DOI
  9. [9]Hussain S. Sajini A.A. Blanco S. Dietmann S. Lombard P. Sugimoto Y. Paramor M. Gleeson J.G. Odom D.T. Ule J. NSun2-mediated cytosine-5 methylation of vault noncoding RNA determines its processing into regulatory small RNAs Cell Rep. 2013 4 255 261 10.1016/j.celrep.2013.06.029 23871666 PMC3730056 · DOI
  10. [10]Yang X. Yang Y. Sun B.-F. Chen Y.-S. Xu J.-W. Lai W.-Y. Li A. Wang X. Bhattarai D.P. Xiao W. 5-methylcytosine promotes mRNA export - NSUN2 as the methyltransferase and ALYREF as an m(5)C reader Cell Res. 2017 27 606 625 10.1038/cr.2017.55 28418038 PMC5594206 · DOI
  11. [11]Tang H. Fan X. Xing J. Liu Z. Jiang B. Dou Y. Gorospe M. Wang W. NSun2 delays replicative senescence by repressing p27 (KIP1) translation and elevating CDK1 translation Aging (Albany. NY). 2015 7 1143 1158 10.18632/aging.100860 26687548 PMC4712338 · DOI
  12. [12]Xing J. Yi J. Cai X. Tang H. Liu Z. Zhang X. Martindale J.L. Yang X. Jiang B. Gorospe M. NSun2 Promotes Cell Growth via Elevating Cyclin-Dependent Kinase 1 Translation Mol. Cell. Biol. 2015 35 4043 4052 10.1128/MCB.00742-15 26391950 PMC4628067 · DOI
  13. [13]Li Q. Li X. Tang H. Jiang B. Dou Y. Gorospe M. Wang W. NSUN2-Mediated m5C Methylation and METTL3/METTL14-Mediated m6A Methylation Cooperatively Enhance p21 Translation J. Cell. Biochem. 2017 118 2587 2598 10.1002/jcb.25957 28247949 PMC5509477 · DOI
  14. [14]Van Haute L. Dietmann S. Kremer L. Hussain S. Pearce S.F. Powell C.A. Rorbach J. Lantaff R. Blanco S. Sauer S. Deficient methylation and formylation of mt-tRNA(Met) wobble cytosine in a patient carrying mutations in NSUN3 Nat. Commun. 2016 7 12039 10.1038/ncomms12039 27356879 PMC4931328 · DOI
  15. [15]Haag S. Sloan K.E. Ranjan N. Warda A.S. Kretschmer J. Blessing C. Hübner B. Seikowski J. Dennerlein S. Rehling P. NSUN3 and ABH1 modify the wobble position of mt-tRNAMet to expand codon recognition in mitochondrial translation Embo J. 2016 35 2104 2119 10.15252/embj.201694885 27497299 PMC5048346 · DOI
  16. [16]Nakano S. Suzuki T. Kawarada L. Iwata H. Asano K. Suzuki T. NSUN3 methylase initiates 5-formylcytidine biogenesis in human mitochondrial tRNAMet Nat. Chem. Biol. 2016 12 546 551 10.1038/nchembio.2099 27214402 · DOI
  17. [17]Metodiev M.D. Spahr H. Loguercio Polosa P. Meharg C. Becker C. Altmueller J. Habermann B. Larsson N.-G. Ruzzenente B. NSUN4 is a dual function mitochondrial protein required for both methylation of 12S rRNA and coordination of mitoribosomal assembly PLoS Genet. 2014 10 e1004110 10.1371/journal.pgen.1004110 24516400 PMC3916286 · DOI
  18. [18]Schosserer M. Minois N. Angerer T.B. Amring M. Dellago H. Harreither E. Calle-Perez A. Pircher A. Gerstl M.P. Pfeifenberger S. Methylation of ribosomal RNA by NSUN5 is a conserved mechanism modulating organismal lifespan Nat. Commun. 2015 6 6158 10.1038/ncomms7158 25635753 PMC4317494 · DOI
  19. [19]Gigova A. Duggimpudi S. Pollex T. Pollex T.I.M. Schaefer M. A cluster of methylations in the domain IV of 25S rRNA is required for ribosome stability A cluster of methylations in the domain IV of 25S rRNA is required for ribosome stability RNA 2014 20 1632 1644 10.1261/rna.043398.113 25125595 PMC4174444 · DOI
  20. [20]Sharma S. Yang J. Watzinger P. Kötter P. Entian K.D. Yeast Nop2 and Rcm1 methylate C2870 and C2278 of the 25S rRNA, respectively Nucleic Acids Res. 2013 41 9062 9076 10.1093/nar/gkt679 23913415 PMC3799443 · DOI
  21. [21]Liu R.-J. Long T. Li J. Li H. Wang E.-D. Structural basis for substrate binding and catalytic mechanism of a human RNA:m5C methyltransferase NSun6 Nucleic Acids Res. 2017 45 6684 6697 10.1093/nar/gkx473 28531330 PMC5499824 · DOI
  22. [22]Haag S. Warda A.S. Kretschmer J. Günnigmann M.A. Höbartner C. Bohnsack M.T. NSUN6 is a human RNA methyltransferase that catalyzes formation of m5C72 in specific tRNAs RNA 2015 21 1532 1543 10.1261/rna.051524.115 26160102 PMC4536315 · DOI
  23. [23]Aguilo F. Li S. Balasubramaniyan N. Sancho A. Benko S. Zhang F. Vashisht A. Rengasamy M. Andino B. Chen C.-H. Deposition of 5-Methylcytosine on Enhancer RNAs Enables the Coactivator Function of PGC-1alpha Cell Rep. 2016 14 479 492 10.1016/j.celrep.2015.12.043 26774474 PMC4731243 · DOI
  24. [24]Goll M.G. Kirpekar F. Maggert K.A. Yoder J.A. Hsieh C.-L. Zhang X. Golic K.G. Jacobsen S.E. Bestor T.H. Methylation of tRNAAsp by the DNA methyltransferase homolog Dnmt2 Science 2006 311 395 398 10.1126/science.1120976 16424344 · DOI
  25. [25]Schaefer M. Pollex T. Hanna K. Tuorto F. Meusburger M. Helm M. Lyko F. RNA methylation by Dnmt2 protects transfer RNAs against stress-induced cleavage Genes Dev. 2010 24 1590 1595 10.1101/gad.586710 20679393 PMC2912555 · DOI
  26. [26]Reid R. Greene P.J. Santi D.V. Exposition of a family of RNA m(5)C methyltransferases from searching genomic and proteomic sequences Nucleic Acids Res. 1999 27 3138 3145 10.1093/nar/27.15.3138 10454610 PMC148540 · DOI
  27. [27]Liu Y. Santi D.V. m5C RNA and m5C DNA methyl transferases use different cysteine residues as catalysts Proc. Natl. Acad. Sci. U. S. A. 2000 97 8263 8265 10.1073/pnas.97.15.8263 10899996 PMC26935 · DOI
  28. [28]King M.Y. Redman K.L. RNA methyltransferases utilize two cysteine residues in the formation of 5-methylcytosine Biochemistry 2002 41 11218 11225 10.1021/bi026055q 12220187 · DOI
  29. [29]King M. Ton D. Redman K.L. A conserved motif in the yeast nucleolar protein Nop2p contains an essential cysteine residue Biochem. J. 1999 337 29 35 10.1042/bj3370029 9854021 PMC1219932 · DOI
  30. [30]Redman K.L. Assembly of protein-RNA complexes using natural RNA and mutant forms of an RNA cytosine methyltransferase Biomacromolecules 2006 7 3321 3326 10.1021/bm051012l 17154459 · DOI
  31. [31]Hussain S. Benavente S.B. Nascimento E. Dragoni I. Kurowski A. Gillich A. Humphreys P. Frye M. The nucleolar RNA methyltransferase Misu (NSun2) is required for mitotic spindle stability J. Cell Biol. 2009 186 27 40 10.1083/jcb.200810180 19596847 PMC2712989 · DOI
  32. [32]Jeltsch A. Beyond Watson and Crick: DNA methylation and molecular enzymology of DNA methyltransferases Chembiochem 2002 3 274 293 10.1002/1439-7633(20020402)3:4<274::AID-CBIC274>3.0.CO;2-S 11933228 · DOI
  33. [33]Cheng X. Structure and function of DNA methyltransferases Annu. Rev. Biophys. Biomol. Struct. 1995 24 293 318 10.1146/annurev.bb.24.060195.001453 7663118 · DOI
  34. [34]Osterman D.G. DePillis G.D. Wu J.C. Matsuda A. Santi D.V. 5-Fluorocytosine in DNA is a mechanism-based inhibitor of HhaI methylase Biochemistry 1988 27 5204 5210 10.1021/bi00414a039 3167042 · DOI
  35. [35]Gabbara S. Bhagwat A.S. The mechanism of inhibition of DNA (cytosine-5-)-methyltransferases by 5-azacytosine is likely to involve methyl transfer to the inhibitor Biochem. J. 1995 307 87 92 10.1042/bj3070087 7536414 PMC1136748 · DOI
  36. [36]Watkins N.J. Bohnsack M.T. The box C/D and H/ACA snoRNPs: Key players in the modification, processing and the dynamic folding of ribosomal RNA Wiley Interdiscip. Rev. RNA 2012 3 397 414 10.1002/wrna.117 22065625 · DOI
  37. [38]Hayrapetyan A. Grosjean H. Helm M. Effect of a quaternary pentamine on RNA stabilization and enzymatic methylation Biol. Chem. 2009 390 851 861 10.1515/BC.2009.096 19558320 · DOI
  38. [39]Motorin Y. Helm M. tRNA stabilization by modified nucleotides Biochemistry 2010 49 4934 4944 10.1021/bi100408z 20459084 · DOI
  39. [40]Sharma S. Lafontaine D.L.J. “View From A Bridge”: A New Perspective on Eukaryotic rRNA Base Modification Trends Biochem. Sci. 2015 40 560 575 10.1016/j.tibs.2015.07.008 26410597 · DOI
  40. [41]Taoka M. Nobe Y. Yamaki Y. Yamauchi Y. Ishikawa H. Takahashi N. Nakayama H. Isobe T. The complete chemical structure of Saccharomyces cerevisiae rRNA: Partial pseudouridylation of U2345 in 25S rRNA by snoRNA snR9 Nucleic Acids Res. 2016 44 8951 8961 10.1093/nar/gkw564 27325748 PMC5062969 · DOI
  41. [42]Hong B. Brockenbrough J.S. Wu P. Aris J.P. Nop2p is required for pre-rRNA processing and 60S ribosome subunit synthesis in yeast Mol. Cell. Biol. 1997 17 378 388 10.1128/MCB.17.1.378 8972218 PMC231762 · DOI
  42. [43]Sloan K.E. Bohnsack M.T. Watkins N.J. The 5S RNP Couples p53 Homeostasis to Ribosome Biogenesis and Nucleolar Stress Cell Rep. 2013 5 237 247 10.1016/j.celrep.2013.08.049 24120868 PMC3808153 · DOI
  43. [44]Meyer B. Wurm J.P. Kotter P. Leisegang M.S. Schilling V. Buchhaupt M. Held M. Bahr U. Karas M. Heckel A. The Bowen-Conradi syndrome protein Nep1 (Emg1) has a dual role in eukaryotic ribosome biogenesis, as an essential assembly factor and in the methylation of Psi1191 in yeast 18S rRNA Nucleic Acids Res. 2011 39 1526 1537 10.1093/nar/gkq931 20972225 PMC3045603 · DOI
  44. [45]Haag S. Kretschmer J. Bohnsack M.T. WBSCR22/Merm1 is required for late nuclear pre-ribosomal RNA processing and mediates N7-methylation of G1639 in human 18S rRNA RNA 2015 21 180 187 10.1261/rna.047910.114 25525153 PMC4338346 · DOI
  45. [46]Schaefer M. Steringer J.P. Lyko F. The Drosophila cytosine-5 methyltransferase Dnmt2 is associated with the nuclear matrix and can access DNA during mitosis PLoS One 2008 3 e1414 10.1371/journal.pone.0001414 18183295 PMC2169302 · DOI
  46. [47]Pais de Barros J.P. Keith G. El Adlouni C. Glasser A.L. Mack G. Dirheimer G. Desgres J. 2’-O-methyl-5-formylcytidine (f5Cm), a new modified nucleotide at the “wobble” of two cytoplasmic tRNAs Leu (NAA) from bovine liver Nucleic Acids Res. 1996 24 1489 1496 10.1093/nar/24.8.1489 8628682 PMC145814 · DOI
  47. [48]Kawarada L. Suzuki T. Ohira T. Hirata S. Miyauchi K. Suzuki T. ALKBH1 is an RNA dioxygenase responsible for cytoplasmic and mitochondrial tRNA modifications Nucleic Acids Res. 2017 45 7401 7415 10.1093/nar/gkx354 28472312 PMC5499545 · DOI
  48. [49]Chan C.T.Y. Pang Y.L.J. Deng W. Babu I.R. Dyavaiah M. Begley T.J. Dedon P.C. Reprogramming of tRNA modifications controls the oxidative stress response by codon-biased translation of proteins Nat. Commun. 2012 3 937 10.1038/ncomms1938 22760636 PMC3535174 · DOI
  49. [50]Shanmugam R. Fierer J. Kaiser S. Helm M. Jurkowski T.P. Jeltsch A. Cytosine methylation of tRNA-Asp by DNMT2 has a role in translation of proteins containing poly-Asp sequences Cell Discov. 2015 1 15010 10.1038/celldisc.2015.10 27462411 PMC4860778 · DOI
  50. [51]Tuorto F. Herbst F. Alerasool N. Bender S. Popp O. Federico G. Reitter S. Liebers R. Stoecklin G. Grone H.-J. The tRNA methyltransferase Dnmt2 is required for accurate polypeptide synthesis during haematopoiesis EMBO J. 2015 34 2350 2362 10.15252/embj.201591382 26271101 PMC4570521 · DOI
  51. [52]Muller M. Hartmann M. Schuster I. Bender S. Thuring K.L. Helm M. Katze J.R. Nellen W. Lyko F. Ehrenhofer-Murray A.E. Dynamic modulation of Dnmt2-dependent tRNA methylation by the micronutrient queuine Nucleic Acids Res. 2015 43 10952 10962 10.1093/nar/gkv980 26424849 PMC4678861 · DOI
  52. [53]Tuorto F. Legrand C. Cirzi C. Federico G. Liebers R. Muller M. Ehrenhofer-Murray A.E. Dittmar G. Grone H.-J. Lyko F. Queuosine-modified tRNAs confer nutritional control of protein translation EMBO J. 2018 37 e99777 10.15252/embj.201899777 30093495 PMC6138434 · DOI
  53. [54]Ehrenhofer-Murray A.E. Cross-Talk between Dnmt2-Dependent tRNA Methylation and Queuosine Modification Biomolecules 2017 7 14 10.3390/biom7010014 PMC5372726 28208632 · DOI
  54. [55]Levitt M. Detailed molecular model for transfer ribonucleic acid Nature 1969 224 759 763 10.1038/224759a0 5361649 · DOI
  55. [56]Vare V.Y.P. Eruysal E.R. Narendran A. Sarachan K.L. Agris P.F. Chemical and Conformational Diversity of Modified Nucleosides Affects tRNA Structure and Function Biomolecules 2017 7 29 10.3390/biom7010029 PMC5372741 28300792 · DOI
  56. [57]Li J. Li H. Long T. Dong H. Wang E.-D. Liu R.-J. Archaeal NSUN6 catalyzes m5C72 modification on a wide-range of specific tRNAs Nucleic Acids Res. 2018 10.1093/nar/gky1236 PMC6393295 30541086 · DOI
  57. [58]Cámara Y. Asin-Cayuela J. Park C.B. Metodiev M.D. Shi Y. Ruzzenente B. Kukat C. Habermann B. Wibom R. Hultenby K. MTERF4 regulates translation by targeting the methyltransferase NSUN4 to the mammalian mitochondrial ribosome Cell Metab. 2011 13 527 539 10.1016/j.cmet.2011.04.002 21531335 · DOI
  58. [59]Dudek J. Rehling P. van der Laan M. Mitochondrial protein import: common principles and physiological networks Biochim. Biophys. Acta 2013 1833 274 285 10.1016/j.bbamcr.2012.05.028 22683763 · DOI
  59. [60]Sloan K.E. Hobartner C. Bohnsack M.T. How RNA modification allows non-conventional decoding in mitochondria Cell Cycle 2017 16 145 146 10.1080/15384101.2016.1235860 27687113 PMC5283808 · DOI
  60. [61]Bilbille Y. Gustilo E.M. Harris K.A. Jones C.N. Lusic H. Kaiser R.J. Delaney M.O. Spremulli L.L. Deiters A. Agris P.F. The human mitochondrial tRNAMet: Structure/function relationship of a unique modification in the decoding of unconventional codons J. Mol. Biol. 2011 406 257 274 10.1016/j.jmb.2010.11.042 21168417 PMC3662834 · DOI
  61. [62]Cantara W.A. Murphy F.V. Demirci H. Agris P.F. Expanded use of sense codons is regulated by modified cytidines in tRNA Proc. Natl. Acad. Sci. U. S. A. 2013 110 10964 10969 10.1073/pnas.1222641110 23781103 PMC3704028 · DOI
  62. [63]Carlile T.M. Rojas-Duran M.F. Zinshteyn B. Shin H. Bartoli K.M. Gilbert W.V. Pseudouridine profiling reveals regulated mRNA pseudouridylation in yeast and human cells Nature 2014 515 143 146 10.1038/nature13802 25192136 PMC4224642 · DOI
  63. [64]Dominissini D. Moshitch-Moshkovitz S. Schwartz S. Salmon-Divon M. Ungar L. Osenberg S. Cesarkas K. Jacob-Hirsch J. Amariglio N. Kupiec M. Topology of the human and mouse m6A RNA methylomes revealed by m6A-seq Nature 2012 485 201 206 10.1038/nature11112 22575960 · DOI · Paper page
  64. [66]Dubin D.T. Taylor R.H. The methylation state of poly A-containing messenger RNA from cultured hamster cells Nucleic Acids Res. 1975 2 1653 1668 10.1093/nar/2.10.1653 1187339 PMC343535 · DOI
  65. [67]Squires J.E. Patel H.R. Nousch M. Sibbritt T. Humphreys D.T. Parker B.J. Suter C.M. Preiss T. Widespread occurrence of 5-methylcytosine in human coding and non-coding RNA Nucleic Acids Res. 2012 40 5023 5033 10.1093/nar/gks144 22344696 PMC3367185 · DOI
  66. [68]Amort T. Rieder D. Wille A. Khokhlova-Cubberley D. Riml C. Trixl L. Jia X.-Y. Micura R. Lusser A. Distinct 5-methylcytosine profiles in poly(A) RNA from mouse embryonic stem cells and brain Genome Biol. 2017 18 1 10.1186/s13059-016-1139-1 28077169 PMC5225599 · DOI
  67. [69]Legrand C. Tuorto F. Hartmann M. Liebers R. Jacob D. Helm M. Lyko F. Statistically robust methylation calling for whole-transcriptome bisulfite sequencing reveals distinct methylation patterns for mouse RNAs Genome Res. 2017 27 1589 1596 10.1101/gr.210666.116 28684555 PMC5580717 · DOI
  68. [70]David R. Burgess A. Parker B. Li J. Pulsford K. Sibbritt T. Preiss T. Searle I.R. Transcriptome-Wide Mapping of RNA 5-Methylcytosine in Arabidopsis mRNAs and Noncoding RNAs Plant Cell 2017 29 445 460 10.1105/tpc.16.00751 28062751 PMC5385953 · DOI
  69. [71]Edelheit S. Schwartz S. Mumbach M.R. Wurtzel O. Sorek R. Transcriptome-wide mapping of 5-methylcytidine RNA modifications in bacteria, archaea, and yeast reveals m5C within archaeal mRNAs PLoS Genet. 2013 9 e1003602 10.1371/journal.pgen.1003602 23825970 PMC3694839 · DOI
  70. [72]Ghanbarian H. Wagner N. Polo B. Baudouy D. Kiani J. Michiels J.-F. Cuzin F. Rassoulzadegan M. Wagner K.-D. Dnmt2/Trdmt1 as Mediator of RNA Polymerase II Transcriptional Activity in Cardiac Growth PLoS One 2016 11 e0156953 10.1371/journal.pone.0156953 27270731 PMC4894585 · DOI
  71. [73]Long T. Li J. Li H. Zhou M. Zhou X.-L. Liu R.-J. Wang E.-D. Sequence-specific and Shape-selective RNA Recognition by the Human RNA 5-Methylcytosine Methyltransferase NSun6 J. Biol. Chem. 2016 291 24293 24303 10.1074/jbc.M116.742569 27703015 PMC5104949 · DOI
  72. [74]Muller S. Windhof I.M. Maximov V. Jurkowski T. Jeltsch A. Forstner K.U. Sharma C.M. Graf R. Nellen W. Target recognition, RNA methylation activity and transcriptional regulation of the Dictyostelium discoideum Dnmt2-homologue (DnmA) Nucleic Acids Res. 2013 41 8615 8627 10.1093/nar/gkt634 23877245 PMC3794594 · DOI
  73. [75]Shanmugam R. Aklujkar M. Schafer M. Reinhardt R. Nickel O. Reuter G. Lovley D.R. Ehrenhofer-Murray A. Nellen W. Ankri S. The Dnmt2 RNA methyltransferase homolog of Geobacter sulfurreducens specifically methylates tRNA-Glu Nucleic Acids Res. 2014 42 6487 6496 10.1093/nar/gku256 24711368 PMC4041430 · DOI
  74. [76]Spahr H. Habermann B. Gustafsson C.M. Larsson N.-G. Hallberg B.M. Structure of the human MTERF4-NSUN4 protein complex that regulates mitochondrial ribosome biogenesis Proc. Natl. Acad. Sci. U. S. A. 2012 109 15253 15258 10.1073/pnas.1210688109 22949673 PMC3458362 · DOI
  75. [77]Yakubovskaya E. Guja K.E. Mejia E. Castano S. Hambardjieva E. Choi W.S. Garcia-Diaz M. Structure of the essential MTERF4:NSUN4 protein complex reveals how an MTERF protein collaborates to facilitate rRNA modification Structure 2012 20 1940 1947 10.1016/j.str.2012.08.027 23022348 PMC3496059 · DOI
  76. [78]Blanco S. Frye M. Role of RNA methyltransferases in tissue renewal and pathology Curr. Opin. Cell Biol. 2014 31 1 7 10.1016/j.ceb.2014.06.006 25014650 PMC4238901 · DOI
  77. [79]Khan M.A. Rafiq M.A. Noor A. Hussain S. Flores J.V. Rupp V. Vincent A.K. Malli R. Ali G. Khan F.S. Mutation in NSUN2, which encodes an RNA methyltransferase, causes autosomal-recessive intellectual disability Am. J. Hum. Genet. 2012 90 856 863 10.1016/j.ajhg.2012.03.023 22541562 PMC3376419 · DOI
  78. [80]Martinez F.J. Lee J.H. Lee J.E. Blanco S. Nickerson E. Gabriel S. Frye M. Al-Gazali L. Gleeson J.G. Whole exome sequencing identifies a splicing mutation in NSUN2 as a cause of a Dubowitz-like syndrome J. Med. Genet. 2012 49 380 385 10.1136/jmedgenet-2011-100686 22577224 PMC4771841 · DOI
  79. [81]Flores J.V. Cordero-Espinoza L. Oeztuerk-Winder F. Andersson-Rolf A. Selmi T. Blanco S. Tailor J. Dietmann S. Frye M. Cytosine-5 RNA Methylation Regulates Neural Stem Cell Differentiation and Motility Stem cell reports 2017 8 112 124 10.1016/j.stemcr.2016.11.014 28041877 PMC5233436 · DOI
  80. [82]Trixl L. Amort T. Wille A. Zinni M. Ebner S. Hechenberger C. Eichin F. Gabriel H. Schoberleitner I. Huang A. RNA cytosine methyltransferase Nsun3 regulates embryonic stem cell differentiation by promoting mitochondrial activity Cell. Mol. Life Sci. 2018 75 1483 1497 10.1007/s00018-017-2700-0 29103146 PMC5852174 · DOI
  81. [83]Chi L. Delgado-Olguin P. Expression of NOL1/NOP2/sun domain (Nsun) RNA methyltransferase family genes in early mouse embryogenesis Gene Expr. Patterns 2013 13 319 327 10.1016/j.gep.2013.06.003 23816522 · DOI
  82. [84]Harris T. Marquez B. Suarez S. Schimenti J. Sperm motility defects and infertility in male mice with a mutation in Nsun7, a member of the Sun domain-containing family of putative RNA methyltransferases Biol. Reprod. 2007 77 376 382 10.1095/biolreprod.106.058669 17442852 · DOI
  83. [85]Khosronezhad N. Colagar A.H. Jorsarayi S.G.A. T26248G-transversion mutation in exon7 of the putative methyltransferase Nsun7 gene causes a change in protein folding associated with reduced sperm motility in asthenospermic men Reprod. Fertil. Dev. 2015 27 471 480 10.1071/RD13371 24384068 · DOI
  84. [86]Khosronezhad N. Hosseinzadeh Colagar A. Mortazavi S.M. The Nsun7 (A11337)-deletion mutation, causes reduction of its protein rate and associated with sperm motility defect in infertile men J. Assist. Reprod. Genet. 2015 32 807 815 10.1007/s10815-015-0443-0 25702163 PMC4429448 · DOI
  85. [87]Doll A. Grzeschik K.H. Characterization of two novel genes, WBSCR20 and WBSCR22, deleted in Williams-Beuren syndrome Cytogenet. Cell Genet. 2001 95 20 27 10.1159/000057012 11978965 · DOI
  86. [88]Delatte B. Wang F. Ngoc L.V. Collignon E. Bonvin E. Deplus R. Calonne E. Hassabi B. Putmans P. Awe S. Transcriptome-wide distribution and function of RNA hydroxymethylcytosine Science 2016 351 282 285 10.1126/science.aac5253 26816380 · DOI
  87. [89]Tardu M. Lin Q. Koutmou K.S. N4-acetylcytidine and 5-formylcytidine are present in Saccharomyces cerevisiae mRNAs bioRxiv 2018

Cited by

Sorted by citations

Authors
Bohnsack, K. E., Höbartner, C., & Bohnsack, M. T.
Affiliations
  • Universitätsmedizin Göttingen (DE)
  • University of Würzburg (DE)
Corresponding author
  • Bohnsack, Katherine E.
  • Höbartner, Claudia
  • Bohnsack, Markus T.
ORCID
Venue
Genes
Publisher
MDPI AG
Published
2019-01-30
Volume
10
Issue
2
Pages
102
ISSN
2073-4425 (ISSN-L)
DOI
10.3390/genes10020102
PMC
PMC6409601
OpenAlex
W2911756720
Cited by
517
References
2
Citations by year
2026: 46 · 2025: 92 · 2024: 79 · 2023: 97 · 2022: 75 · 2021: 88 · 2020: 30 · 2019: 10
FWCI
4.50
Type
journal article
Language
en
Open access
Licence
Locations
  • Genes (publishedVersion, cc-by)
  • Europe PMC (PubMed Central) (publishedVersion, cc-by)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
  • DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion)
  • GoeScholar The Publication Server of the Georg-August-Universität Göttingen (Georg-August-Universität Göttingen) (submittedVersion, cc-by)
Funders
Deutsche Forschungsgemeinschaft (BO3442/2-2, HO4426/2-2)
Topics
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › RNA modifications and cancer
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › RNA regulation and disease
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Epigenetics and DNA Methylation
Keywords
5-methylcytosine, RNA methylation, RNA methyltransferase, DNMT2, ribosomal RNA methylation, enhancer RNA, non-coding RNA, target specificity, mitochondrial gene expression, nuclear gene expression, disease
MeSH terms
Animals, Humans, Methyltransferases, RNA Processing, Post-Transcriptional, 5-Methylcytosine, Neurodevelopmental Disorders

About these checks

Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.

Statistics and arithmetic are recomputed, not judged.

Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.

What counts as a claim ›How we measure confidence ›How we check this ›

Are you an author, or do you see a problem with this page? Request a review