Reviving the RNA World: An Insight into the Appearance of RNA Methyltransferases

RNA, the earliest genetic and catalytic molecule, has a relatively delicate and labile chemical structure, when compared to DNA. It is prone to be damaged by alkali, heat, nucleases, or stress conditions. One mechanism to protect RNA or DNA from damage is through site-specific methylation. Here, we propose that RNA methylation began prior to DNA methylation in the early forms of life evolving on Earth. In this article, the biochemical properties of some RNA methyltransferases (MTases), such as 2′-O-MTases (Rlml/RlmN), spOUT MTases and the NSun2 MTases are dissected for the insight they provide on the transition from an RNA world to our present RNA/DNA/protein world.

[1]  L. Mcdaniel,et al.  High Frequency of Horizontal Gene Transfer in the Oceans , 2010, Science.

[2]  P. Holliger,et al.  In-ice evolution of RNA polymerase ribozyme activity. , 2013, Nature chemistry.

[3]  R. Shapiro.  Prebiotic ribose synthesis: A critical analysis , 1986, Origins of life and evolution of the biosphere.

[4]  D. A. Usher,et al.  Hydrolytic stability of helical RNA: a selective advantage for the natural 3',5'-bond. , 1976, Proceedings of the National Academy of Sciences of the United States of America.

[5]  D. Low,et al.  Roles of DNA Adenine Methylation in Regulating Bacterial Gene Expression and Virulence , 2001, Infection and Immunity.

[6]  T. Steitz,et al.  Structure of T 7 RNA polymerase complexed to the transcriptional inhibitor T 7 lysozyme , 2013 .

[7]  Carlos Briones,et al.  Modular evolution and increase of functional complexity in replicating RNA molecules. , 2006, RNA.

[8]  Izabela Makałowska,et al.  Identification of human tRNA:m5C methyltransferase catalysing intron-dependent m5C formation in the first position of the anticodon of the pre-tRNA(CAA)Leu , 2006, Nucleic acids research.

[9]  D. Bartel,et al.  RNA-Catalyzed RNA Polymerization: Accurate and General RNA-Templated Primer Extension , 2001, Science.

[10]  Andrew D. Ellington,et al.  The Robustness of Naturally and Artificially Selected Nucleic Acid Secondary Structures , 2004, Journal of Molecular Evolution.

[11]  P. Schimmel,et al.  Possible role of aminoacyl-RNA complexes in noncoded peptide synthesis and origin of coded synthesis. , 1994, Proceedings of the National Academy of Sciences of the United States of America.

[12]  T. V. Mishanina,et al.  Mechanisms and inhibition of uracil methylating enzymes. , 2012, Bioorganic chemistry.

[13]  M. Schrader.  The RNA world: Conditions for prebiotic synthesis , 2009 .

[14]  D. Penny,et al.  The Path from the RNA World , 1998, Journal of Molecular Evolution.

[15]  A. Lazcano,et al.  The origin of life—did it occur at high temperatures? , 2004, Journal of Molecular Evolution.

[16]  A. Jeltsch,et al.  Two substrates are better than one: dual specificities for Dnmt2 methyltransferases. , 2006, Trends in biochemical sciences.

[17]  M B Sporn,et al.  2'-O-methylation of adenosine, guanosine, uridine, and cytidine in RNA of isolated rat liver nuclei. , 1972, Proceedings of the National Academy of Sciences of the United States of America.

[18]  T. Cech,et al.  Self-splicing RNA: Autoexcision and autocyclization of the ribosomal RNA intervening sequence of tetrahymena , 1982, Cell.

[19]  M. Levy,et al.  The stability of the RNA bases: implications for the origin of life. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[20]  A. Benítez-Páez,et al.  The Escherichia coli RlmN methyltransferase is a dual-specificity enzyme that modifies both rRNA and tRNA and controls translational accuracy. , 2012, RNA.

[21]  S L Miller,et al.  Investigation of the prebiotic synthesis of amino acids and RNA bases from CO2 using FeS/H2S as a reducing agent. , 1995, Proceedings of the National Academy of Sciences of the United States of America.

[22]  M. Tatsuka,et al.  Aurora-B regulates RNA methyltransferase NSUN2. , 2007, Molecular biology of the cell.

[23]  Eugene V. Koonin,et al.  Virus World as an Evolutionary Network of Viruses and Capsidless Selfish Elements , 2014, Microbiology and Molecular Reviews.

[24]  E. Meléndez-Hevia.  From the RNA world to the DNA-protein world: clues to the origin and early evolution of life in the ribosome , 2009, Journal of Biosciences.

[25]  L. Orgel,et al.  Prebiotic chemistry and the origin of the RNA world. , 2004, Critical reviews in biochemistry and molecular biology.

[26]  Eugene V Koonin,et al.  Comparative genomics and evolution of proteins involved in RNA metabolism. , 2002, Nucleic acids research.

[27]  Justin L Cotney,et al.  Evidence for an Early Gene Duplication Event in the Evolution of the Mitochondrial Transcription Factor B Family and Maintenance of rRNA Methyltransferase Activity in Human mtTFB1 and mtTFB2 , 2006, Journal of Molecular Evolution.

[28]  S. Miller,et al.  Prebiotic Synthesis of Methionine , 1972, Science.

[29]  P. Reichard,et al.  From RNA to DNA, why so many ribonucleotide reductases? , 1993, Science.

[30]  T. Eickbush,et al.  Origin and evolution of retroelements based upon their reverse transcriptase sequences. , 1990, The EMBO journal.

[31]  N. Lehman,et al.  The RNA World: molecular cooperation at the origins of life , 2014, Nature Reviews Genetics.

[32]  David P. Bartel,et al.  RNA-catalysed RNA polymerization using nucleoside triphosphates , 1996, Nature.

[33]  Xiaoyu Zhang,et al.  Methylation of tRNAAsp by the DNA Methyltransferase Homolog Dnmt2 , 2006, Science.

[34]  L. Kirsebom,et al.  The naturally trans-acting ribozyme RNase P RNA has leadzyme properties , 2005, Nucleic acids research.

[35]  J. Ferris,et al.  Montmorillonite catalysis of RNA oligomer formation in aqueous solution. A model for the prebiotic formation of RNA. , 1993, Journal of the American Chemical Society.

[36]  Marcin Feder,et al.  Sequence-structure-function studies of tRNA:m5C methyltransferase Trm4p and its relationship to DNA:m5C and RNA:m5U methyltransferases. , 2004, Nucleic acids research.

[37]  I. Ivanov,et al.  Non-Enzymatic RNA Hydrolysis Promoted by the Combined Catalytic Activity of Buffers and Magnesium Ions , 1999, Zeitschrift fur Naturforschung. C, Journal of biosciences.

[38]  John M. Walker,et al.  Comparative Genomics , 2007, Methods In Molecular Biology™.

[39]  Ricardo Flores,et al.  Viroids: the minimal non‐coding RNAs with autonomous replication , 2004, FEBS letters.

[40]  Francesca Tuorto,et al.  RNA methylation by Dnmt2 protects transfer RNAs against stress-induced cleavage. , 2010, Genes & development.

[41]  R J Roberts,et al.  On base flipping , 1995, Cell.

[42]  T. Steitz,et al.  Structure of T7 RNA polymerase complexed to the transcriptional inhibitor T7 lysozyme , 1998, The EMBO journal.

[43]  U. Müller,et al.  Re-creating an RNA world , 2006, Cellular and Molecular Life Sciences CMLS.

[44]  J. V. Van Etten,et al.  Cloning and sequencing the cytosine methyltransferase gene M. CviJI from Chlorella virus IL-3A. , 1990, Virology.

[45]  J. Perona,et al.  Stereochemical mechanisms of tRNA methyltransferases , 2010, FEBS letters.

[46]  P. Sergiev,et al.  The last rRNA methyltransferase of E. coli revealed: the yhiR gene encodes adenine-N6 methyltransferase specific for modification of A2030 of 23S ribosomal RNA. , 2012, RNA.

[47]  A. Jeltsch,et al.  The Human Dnmt2 Has Residual DNA-(Cytosine-C5) Methyltransferase Activity* , 2003, Journal of Biological Chemistry.

[48]  Julie A. Law,et al.  Establishing, maintaining and modifying DNA methylation patterns in plants and animals , 2010, Nature Reviews Genetics.

[49]  C. Gaspin,et al.  Two different mechanisms for tRNA ribose methylation in Archaea: a short survey. , 2005, Biochimie.

[50]  C. Krebs,et al.  A Radically Different Mechanism for S-Adenosylmethionine–Dependent Methyltransferases , 2011, Science.

[51]  Dagmar Wieczorek,et al.  Mutations in NSUN2 cause autosomal-recessive intellectual disability. , 2012, American journal of human genetics.

[52]  Stanley L. Miller,et al.  An efficient prebiotic synthesis of cytosine and uracil , 1995, Nature.

[53]  K. Bourtzis,et al.  Wolbachia Prophage DNA Adenine Methyltransferase Genes in Different Drosophila-Wolbachia Associations , 2011, PloS one.

[54]  L. Shapiro,et al.  The CcrM DNA methyltransferase is widespread in the alpha subdivision of proteobacteria, and its essential functions are conserved in Rhizobium meliloti and Caulobacter crescentus , 1997, Journal of bacteriology.

[55]  Z. Cui,et al.  A peptidyl transferase ribozyme capable of combinatorial peptide synthesis. , 2004, Bioorganic & medicinal chemistry.

[56]  G. F. Joyce,et al.  Self-Sustained Replication of an RNA Enzyme , 2009, Science.

[57]  A. Jeltsch,et al.  Horizontal gene transfer contributes to the wide distribution and evolution of type II restriction-modification systems , 1996, Journal of Molecular Evolution.

[58]  J. Goodchild.  Enhancement of ribozyme catalytic activity by a contiguous oligodeoxynucleotide (facilitator) and by 2'-O-methylation. , 1992, Nucleic acids research.

[59]  G. Caetano-Anollés,et al.  Ribosomal History Reveals Origins of Modern Protein Synthesis , 2012, PloS one.

[60]  S. Miller.  A production of amino acids under possible primitive earth conditions. , 1953, Science.

[61]  Albert Jeltsch,et al.  Human DNMT2 methylates tRNA(Asp) molecules using a DNA methyltransferase-like catalytic mechanism. , 2008, RNA.

[62]  H. Lodish,et al.  The Three Roles of RNA in Protein Synthesis , 2000 .

[63]  Stanley L. Miller,et al.  Organic Compound Synthes on the Primitive Eart: Several questions about the origin of life have been answered, but much remains to be studied , 1959 .

[64]  O. Nureki,et al.  The Catalytic Domain of Topological Knot tRNA Methyltransferase (TrmH) Discriminates between Substrate tRNA and Nonsubstrate tRNA via an Induced-fit Process* , 2013, The Journal of Biological Chemistry.

[65]  B. Golinelli‐Pimpaneau,et al.  Dynamics of RNA modification by a multi-site-specific tRNA methyltransferase , 2014, Nucleic acids research.

[66]  B. Sjöberg,et al.  Methyl-RNA: an evolutionary bridge between RNA and DNA? , 2000, Chemistry & Biology.

[67]  C Gaspin,et al.  Box C/D RNA guides for the ribose methylation of archaeal tRNAs. The tRNATrp intron guides the formation of two ribose-methylated nucleosides in the mature tRNATrp. , 2001, Nucleic acids research.

[68]  C. Crestini,et al.  Nucleoside Phosphorylation by Phosphate Minerals* , 2007, Journal of Biological Chemistry.

[69]  P. Schimmel,et al.  Peptide synthesis with a template-like RNA guide and aminoacyl phosphate adaptors , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[70]  A. Ferré-D’Amaré,et al.  Small self-cleaving ribozymes. , 2010, Cold Spring Harbor perspectives in biology.

[71]  Joanna M. Kasprzak,et al.  Crystal structure of the Escherichia coli 23S rRNA:m5C methyltransferase RlmI (YccW) reveals evolutionary links between RNA modification enzymes. , 2008, Journal of molecular biology.

[72]  Jakub Pas,et al.  Molecular phylogenetics of the RrmJ/fibrillarin superfamily of ribose 2'-O-methyltransferases. , 2003, Gene.

[73]  S. Miller,et al.  The atmosphere of the primitive earth and the prebiotic synthesis of organic compounds. , 1983, Advances in space research : the official journal of the Committee on Space Research.

[74]  Jernej Ule,et al.  Aberrant methylation of tRNAs links cellular stress to neuro-developmental disorders , 2014, The EMBO journal.

[75]  D Penny,et al.  Pre-rRNA processing and the path from the RNA world. , 1995, Trends in biochemical sciences.

[76]  H. Sasaki,et al.  Accumulation and loss of asymmetric non-CpG methylation during male germ-cell development , 2012, Nucleic acids research.

[77]  J. Stubbe.  The Two Faces of SAM , 2011, Science.

[78]  C. Kurland,et al.  Horizontal gene transfer: A critical view , 2003 .

[79]  A. Lamond,et al.  Nuclease resistant ribozymes with high catalytic activity. , 1992, The EMBO journal.

[80]  Z. Cui,et al.  A selected ribozyme catalyzing diverse dipeptide synthesis. , 2002, Chemistry & biology.

[81]  S. Duthie,et al.  Impact of folate deficiency on DNA stability. , 2002, The Journal of nutrition.

[82]  A. Jeltsch,et al.  On the Evolutionary Origin of Eukaryotic DNA Methyltransferases and Dnmt2 , 2011, PloS one.

[83]  Hani S. Zaher,et al.  Selection of an improved RNA polymerase ribozyme with superior extension and fidelity. , 2007, RNA.

[84]  O. Uhlenbeck,et al.  Self‐cleaving catalytic RNA , 1993, FASEB journal : official publication of the Federation of American Societies for Experimental Biology.

[85]  E. Wang,et al.  The tRNA recognition mechanism of the minimalist SPOUT methyltransferase, TrmL , 2013, Nucleic acids research.

[86]  Wen Liu,et al.  Radical-Mediated Enzymatic Methylation: A Tale of Two SAMS , 2011, Accounts of chemical research.

[87]  J. Dworkin,et al.  Alternative bases in the RNA world: The prebiotic synthesis of urazole and its ribosides , 2004, Journal of Molecular Evolution.

[88]  Ichiro Hirao,et al.  Re-creating the RNA world , 1995, Current Biology.

[89]  Ronald R. Breaker,et al.  In vitro selection of self-cleaving DNAs. , 1996, Chemistry & biology.

[90]  Y. Tsukada.  Hydroxylation mediates chromatin demethylation. , 2012, Journal of biochemistry.

[91]  Jernej Ule,et al.  NSun2-Mediated Cytosine-5 Methylation of Vault Noncoding RNA Determines Its Processing into Regulatory Small RNAs , 2013, Cell reports.

[92]  J. Steitz,et al.  A general two-metal-ion mechanism for catalytic RNA. , 1993, Proceedings of the National Academy of Sciences of the United States of America.

[93]  R. Stroud,et al.  Structure of a TrmA–RNA complex: A consensus RNA fold contributes to substrate selectivity and catalysis in m5U methyltransferases , 2008, Proceedings of the National Academy of Sciences.

[94]  Y. Tor,et al.  Hydrolytic Fitness of N-glycosyl Bonds: Comparing the Deglycosylation Kinetics of Modified, Alternative and Native Nucleosides. , 2015, Journal of physical organic chemistry.

[95]  D. Crook,et al.  Genomic islands: tools of bacterial horizontal gene transfer and evolution , 2008, FEMS microbiology reviews.

[96]  G. Cooper.  The Origin and Evolution of Cells , 2000 .

[97]  J. Bada,et al.  Prebiotic Synthesis of Methionine and Other Sulfur-Containing Organic Compounds on the Primitive Earth: A Contemporary Reassessment Based on an Unpublished 1958 Stanley Miller Experiment , 2010, Origins of Life and Evolution of Biospheres.

[98]  A Dnmt2-like protein mediates DNA methylation in Drosophila , 2003, Development.

[99]  H. Urey,et al.  Organic compound synthesis on the primitive earth. , 1959, Science.

[100]  P. Schimmel,et al.  Oligonucleotide-directed peptide synthesis in a ribosome- and ribozyme-free system. , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[101]  X. Zhuang,et al.  Functional importance of telomerase pseudoknot revealed by single-molecule analysis , 2011, Proceedings of the National Academy of Sciences.

[102]  Y. Motorin,et al.  Multisite-specific tRNA:m5C-methyltransferase (Trm4) in yeast Saccharomyces cerevisiae: identification of the gene and substrate specificity of the enzyme. , 1999, RNA.

[103]  J. Perona,et al.  Mechanism of N-methylation by the tRNA m1G37 methyltransferase Trm5. , 2010, RNA.

[104]  A. Brennicke,et al.  A mitochondrial rRNA dimethyladenosine methyltransferase in Arabidopsis , 2010, The Plant journal : for cell and molecular biology.

[105]  B. Golinelli‐Pimpaneau,et al.  The human tRNA m5C methyltransferase Misu is multisite-specific , 2012, RNA biology.

[106]  Frank Lyko,et al.  Solving the Dnmt2 enigma , 2010, Chromosoma.

[107]  B. Ganem.  RNA world , 1987, Nature.

[108]  J W Szostak,et al.  Ribozymes: aiming at RNA replication and protein synthesis. , 1996, Chemistry & biology.

[109]  L. Gold,et al.  In vitro selection of self-cleaving RNAs with a low pH optimum. , 1997, Proceedings of the National Academy of Sciences of the United States of America.

[110]  N. Zenkin.  Hypothesis: Emergence of Translation as a Result of RNA Helicase Evolution , 2012, Journal of Molecular Evolution.

[111]  D. Bartel,et al.  The structural basis of RNA-catalyzed RNA polymerization , 2011, Nature Structural &Molecular Biology.

[112]  T. Nozaki,et al.  The Entamoeba histolytica Dnmt2 Homolog (Ehmeth) Confers Resistance to Nitrosative Stress , 2014, Eukaryotic Cell.

[113]  W. Stemmer,et al.  Breeding of retroviruses by DNA shuffling for improved stability and processing yields , 2000, Nature Biotechnology.

[114]  Irene A. Chen,et al.  The RNA World as a Model System to Study the Origin of Life , 2015, Current Biology.