Posttranscriptional methylation of transfer and ribosomal RNA in stress response pathways, cell differentiation, and cancer

Current Opinion in Oncology

Volumn 28, Issue 1, 2016, Pages 65-71

  Popis, Martyna C ^a   Blanco, Sandra ^a   Frye, Michaela ^a  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

Author keywords

Cancer; cellular stress response; cytosine 5 methylation; noncoding RNA; NSun proteins; stem cells

Indexed keywords

5 METHYLCYTIDINE; CYTIDINE DERIVATIVE; CYTOSINE; CYTOSINE 5; RIBOSOME RNA; UNCLASSIFIED DRUG; UNTRANSLATED RNA; 5-METHYLCYTIDINE; CYTIDINE; METHYLTRANSFERASE; NSUN4 PROTEIN, HUMAN;

CANCER GROWTH; CELL DIFFERENTIATION; CELL FATE; CELLULAR STRESS RESPONSE; CHEMICAL MODIFICATION; HUMAN; MALIGNANT NEOPLASTIC DISEASE; NONHUMAN; POSTTRANSCRIPTIONAL METHYLATION; PRIORITY JOURNAL; REVIEW; RNA METHYLATION; RNA TRANSPORT; TRANSLATION INITIATION; ANALOGS AND DERIVATIVES; GENETICS; METABOLISM; METHYLATION; NEOPLASM; PATHOLOGY; PHYSIOLOGICAL STRESS; PHYSIOLOGY; RNA PROCESSING;

CELL DIFFERENTIATION; CYTIDINE; CYTOSINE; HUMANS; METHYLATION; METHYLTRANSFERASES; NEOPLASMS; RNA PROCESSING, POST-TRANSCRIPTIONAL; RNA, RIBOSOMAL; STRESS, PHYSIOLOGICAL;

EID: 84951569387     PISSN: 10408746     EISSN: 1531703X     Source Type: Journal    
DOI: 10.1097/CCO.0000000000000252     Document Type: Review

References (96)

1. Gangaraju VK, Lin H. MicroRNAs: key regulators of stem cells. Nat Rev Mol Cell Biol 2009; 10:116-125.
2. Kanellopoulou C, et al. Dicer-deficient mouse embryonic stem cells are defective in differentiation and centromeric silencing. Genes Dev 2005; 19:489-501.
3. Wang Y, et al. DGCR8 is essential for microRNA biogenesis and silencing of embryonic stem cell self-renewal. Nat Genet 2007; 39:380-385.
4. Machnicka MA, et al. MODOMICS: a database of RNA modification pathways: 2013 update. Nucleic Acids Res 2013; 41 (Database issue):D262-D267.
5. Cantara WA, et al. The RNA modification database, RNAMDB: 2011 update. Nucleic Acids Res 2011; 39:D195-201.
6. Towns WL, Begley TJ. Transfer RNA methytransferases and their corresponding modifications in budding yeast and humans: activities, predications, and potential roles in human health. DNA Cell Biol 2012; 31:434-454.
7. Bujnicki JM, et al. Sequence-structure-function studies of tRNA:m5C methyltransferase Trm4p and its relationship to DNA:m5C and RNA:m5U methyltransferases. Nucleic Acids Res 2004; 32:2453-2463.
8. Motorin Y, Lyko F, Helm M. 5-methylcytosine in RNA: detection, enzymatic formation and biological functions. Nucleic Acids Res 2010; 38:1415-1430.
9. Burgess AL, David R, Searle IR. Conservation of tRNA and rRNA 5-methylcytosine in the kingdom Plantae. BMC Plant Biol 2015; 15:199.
10. Gold M, Hurwitz J, Anders M. The enzymatic methylation of RNA and DNA, II. On the species specificity of the methylation enzymes. Proc Natl Acad Sci USA 1963; 50:164-169.
11. Dubin DT, Taylor RH. The methylation state of poly A-containing messenger RNA from cultured hamster cells. Nucleic Acids Res 1975; 2:1653-1668.
12. Wei CM, Gershowitz A, Moss B. Methylated nucleotides block 50 terminus of HeLa cell messenger RNA. Cell 1975; 4:379-386.
13. Perry RP, et al. The methylated constituents of L cell messenger RNA: evidence for an unusual cluster at the 50 terminus. Cell 1975; 4:387-394.
14. Bokar JA. The biosynthesis and functional roles of methylated nucleosides in eukaryotic mRNA. In: Grosjean H, editor. Fine-tuning of RNA functions by modification and editing. Berlin: Springer; 2005. pp. 141-177.
15. Hussain S, et al. Characterizing 5-methylcytosine in the mammalian epitranscriptome. Genome Biol 2013; 14:215.
16. Meyer KD, et al. Comprehensive analysis of mRNA methylation reveals enrichment in 30 UTRs and near stop codons. Cell 2012; 149:1635-1646.
17. Dominissini D, et al. Topology of the human and mouse m6A RNA methylomes revealed by m6A-seq. Nature 2012; 485:201-206.
18. Hussain S, et al. NSun2-mediated cytosine-5 methylation of vault noncoding RNA determines its processing into regulatory small RNAs. Cell Rep 2013; 4:255-261.
19. Squires JE, et al. Widespread occurrence of 5-methylcytosine in human coding and noncoding RNA. Nucleic Acids Res 2012; 40:5023-5033.
20. Somers J, Poyry T, Willis AE. A perspective on mammalian upstream open reading frame function. Int J Biochem Cell Biol 2013; 45:1690-1700.
21. Khoddami V, Cairns BR. Identification of direct targets and modified bases of RNA cytosine methyltransferases. Nat Biotechnol 2013; 31:458-464.
22. Schwartz S, et al. High-resolution mapping reveals a conserved, widespread, dynamic mRNA methylation program in yeast meiosis. Cell 2013; 155:1409-1421.
23. Blanco S, Frye M. Role of RNA methyltransferases in tissue renewal and pathology. Curr Opin Cell Biol 2014; 31:1-7.
24. Yue Y, Liu J, He C. RNA N6-methyladenosine methylation in posttranscriptional gene expression regulation. Genes Dev 2015; 29:1343-1355.
25. Sarin LP, Leidel SA. Modify or die RNA modification defects in metazoans. RNA Biol 2014; 11:1555-1567.
26. Lee M, Kim B, Kim VN. Emerging roles of RNA modification: m(6)A and U-tail. Cell 2014; 158:980-987.
27. Meyer KD, Jaffrey SR. The dynamic epitranscriptome: N6-methyladenosine and gene expression control. Nat Rev Mol Cell Biol 2014; 15:313-326.
28. Wang X, He C. Reading RNA methylation codes through methyl-specific binding proteins. RNA Biol 2014; 11:669-672.
29. Chandola U, Das R, Panda B. Role of the N6-methyladenosine RNA mark in gene regulation and its implications on development and disease. Brief Funct Genomics 2015; 14:169-179.
30. King MY, Redman KL. RNA methyltransferases utilize two cysteine residues in the formation of 5-methylcytosine. Biochemistry 2002; 41:11218-11225.
31. Liu Y, Santi DV. m5C RNA and m5C DNA methyl transferases use different cysteine residues as catalysts. Proc Natl Acad Sci USA 2000; 97:8263-8265.
32. Redman KL. Assembly of protein-RNA complexes using natural RNA and mutant forms of an RNA cytosine methyltransferase. Biomacromolecules 2006; 7:3321-3326.
33. Goll MG, et al. Methylation of tRNAAsp by the DNA methyltransferase homolog Dnmt2. Science 2006; 311:395-398.
34. Brzezicha B, et al. Identification of human tRNA:m5C methyltransferase catalysing intron-dependent m5C formation in the first position of the anticodon of the pretRNA Leu (CAA). Nucleic Acids Res 2006; 34:6034-6043.
35. Haag S, et al. NSUN6 is a human RNA methyltransferase that catalyzes formation of m5C72 in specific tRNAs. RNA 2015; 21:1532-1543.
36. Schosserer M, et al. Methylation of ribosomal RNA by NSUN5 is a conserved mechanism modulating organismal lifespan. Nat Commun 2015; 6:6158.
37. Yakubovskaya E, et al. Structure of the essential MTERF4:NSUN4 protein complex reveals how an MTERF protein collaborates to facilitate rRNA modification. Structure 2012; 20:1940-1947.
38. Metodiev MD, et al. NSUN4 is a dual function mitochondrial protein required for both methylation of 12S rRNA and coordination of mitoribosomal assembly. PLoS Genet 2014; 10:e1004110.
39. Tuorto F, et al. RNA cytosine methylation by Dnmt2 and NSun2 promotes tRNA stability and protein synthesis. Nat Struct Mol Biol 2012; 19:900-905.
40. Blanco S, et al. Aberrant methylation of tRNAs links cellular stress to neurodevelopmental disorders. EMBO J 2014; 33:2020-2039.
41. Sharma S, et al. Yeast Nop2 and Rcm1 methylate C2870 and C2278 of the 25S rRNA, respectively. Nucleic Acids Res 2013; 41:9062-9076.
42. Gigova A, et al. A cluster of methylations in the domain IV of 25S rRNA is required for ribosome stability. RNA 2014; 20:1632-1644.
43. Bourgeois G, et al. Eukaryotic rRNA modification by yeast 5-methylcytosinemethyltransferases and human proliferation-associated antigen p120. PLoS One 2015; 10:e0133321.
44. Ramani AK, et al. A map of human protein interactions derived from coexpression of human mRNAs and their orthologs. Mol Syst Biol 2008; 4:180.
45. Schaefer M, et al. RNA methylation by Dnmt2 protects transfer RNAs against stress-induced cleavage. Genes Dev 2010; 24:1590-1595.
46. Ivanov P, et al. Angiogenin-induced tRNA fragments inhibit translation initiation. Mol Cell 2011; 43:613-623.
47. Spriggs KA, Bushell M, Willis AE. Translational regulation of gene expression during conditions of cell stress. Mol Cell 2010; 40:228-237.
48. Sobala A, Hutvagner G. Small RNAs derived from the 50 end of tRNA can inhibit protein translation in human cells. RNA Biol 2013; 10:553-563.
49. Gebetsberger J, et al. tRNA-derived fragments target the ribosome and function as regulatory noncoding RNA in Haloferax volcanii. Archaea 2012; 2012:260909.
50. Tuorto F, et al. The tRNA methyltransferase Dnmt2 is required for accurate polypeptide synthesis during haematopoiesis. EMBOJ 2015; 34:2350-2362.
51. Nevins TA, et al. Distinct regulation of internal ribosome entry site-mediated translation following cellular stress is mediated by apoptotic fragments of eIF4G translation initiation factor family members eIF4GI and p97/DAP5/NAT1. J Biol Chem 2003; 278:3572-3579.
52. Gerashchenko MV, Lobanov AV, Gladyshev VN. Genome-wide ribosome profiling reveals complex translational regulation in response to oxidative stress. Proc Natl Acad Sci USA 2012; 109:17394-17399.
53. Sonenberg N, Hinnebusch AG. Regulation of translation initiation in eukaryotes: mechanisms and biological targets. Cell 2009; 136:731-745.
54. Spriggs KA, et al. Re-programming of translation following cell stress allows IRES-mediated translation to predominate. Biol Cell 2008; 100:27-38.
55. Khan MA, et al. Mutation in NSUN2, which encodes an RNA methyltransferase, causes autosomal-recessive intellectual disability. Am J Hum Genet 2012; 90:856-863.
56. Martinez FJ, et al. Whole exome sequencing identifies a splicing mutation in NSUN2 as a cause of a Dubowitz-like syndrome. J Med Genet 2012; 49:380-385.
57. Abbasi-Moheb L, et al. Mutations in NSUN2 cause autosomal-recessive intellectual disability. Am J Hum Genet 2012; 90:847-855.
58. Komara M, et al. A Novel single-nucleotide deletion (c.1020delA) in NSUN2 causes intellectual disability in an Emirati child. J Mol Neurosci 2015; 57:393-399.
59. Blanco S, et al. The RNA-methyltransferase Misu (NSun2) poises epidermal stem cells to differentiate. PLoS Genet 2011; 7:e1002403.
60. Hussain S, et al. The mouse cytosine-5 RNA methyltransferase NSun2 is a component of the chromatoid body and required for testis differentiation. Mol Cell Biol 2013; 33:1561-1570.
61. Rai K, et al. Dnmt2 functions in the cytoplasm to promote liver, brain, and retina development in zebrafish. Genes Dev 2007; 21:261-266.
62. Bartok O, et al. Adaptation of molecular circadian clockwork to environmental changes: a role for alternative splicing and miRNAs. Proc Biol Sci 2013; 280:20130011.
63. Helm M, Alfonzo JD. Posttranscriptional RNA modifications: playing metabolic games in a cell's chemical Legoland. Chem Biol 2014; 21:174-185.
64. Wu P, et al. NCL1, a novel gene for a nonessential nuclear protein in Saccharomyces cerevisiae. Gene 1998; 220 (1-2):109-117.
65. Chernyakov I, et al. Degradation of several hypomodified mature tRNA species in Saccharomyces cerevisiae is mediated by Met22 and the 50-30 exonucleases Rat1 and Xrn1. Genes Dev 2008; 22:1369-1380.
66. Okamoto M, et al. tRNA modifying enzymes, NSUN2 and METTL1, determine sensitivity to 5-fluorouracil in HeLa cells. PLoS Genet 2014; 10:e1004639.
67. Thompson DM, Parker R. Stressing out over tRNA cleavage. Cell 2009; 138:215-219.
68. Thompson DM, et al. tRNA cleavage is a conserved response to oxidative stress in eukaryotes. RNA 2008; 14:2095-2103.
69. Fu H, et al. Stress induces tRNA cleavage by angiogenin in mammalian cells. FEBS Lett 2009; 583:437-442.
70. Chan CT, et al. A quantitative systems approach reveals dynamic control of tRNA modifications during cellular stress. PLoS Genet 2010; 6:e1001247.
71. Yamasaki S, et al. Angiogenin cleaves tRNA and promotes stress-induced translational repression. J Cell Biol 2009; 185:35-42.
72. Wek RC, Jiang HY, Anthony TG. Coping with stress: eIF2 kinases and translational control. Biochem Soc Trans 2006; 34 (Pt 1):7-11.
73. Jack K, et al. rRNA pseudouridylation defects affect ribosomal ligand binding and translational fidelity from yeast to human cells. Mol Cell 2011; 44:660-666.
74. Endres L, Dedon PC, Begley TJ. Codon-biased translation can be regulated by wobble-base tRNA modification systems during cellular stress responses. RNA Biol 2015; 12:603-614.
75. Chan CT, et al. Reprogramming of tRNA modifications controls the oxidative stress response by codon-biased translation of proteins. Nat Commun 2012; 3:937.
76. Ingolia NT, et al. Genome-wide analysis in vivo of translation with nucleotide resolution using ribosome profiling. Science 2009; 324:218-223.
77. Vesper O, et al. Selective translation of leaderless mRNAs by specialized ribosomes generated by MazF in Escherichia coli. Cell 2011; 147:147-157.
78. Grewal SS. Why should cancer biologists care about tRNAs tRNA synthesis, mRNA translation and the control of growth. Biochim Biophys Acta 2015; 1849:898-907.
79. Kirchner S, Ignatova Z. Emerging roles of tRNA in adaptive translation, signalling dynamics and disease. Nat Rev Genet 2015; 16:98-112.
80. Lee YS, et al. A novel class of small RNAs: tRNA-derived RNA fragments (tRFs). Genes Dev 2009; 23:2639-2649.
81. Honda S, et al. Sex hormone-dependent tRNA halves enhance cell proliferation in breast and prostate cancers. Proc Natl Acad Sci USA 2015; 112:E3816-E3825.
82. Goodarzi H, et al. Endogenous tRNA-derived fragments suppress breast cancer progression via YBX1 displacement. Cell 2015; 161:790-802.
83. Ruggero D. Translational control in cancer etiology. Cold Spring Harb Perspect Biol 2013; 5.
84. Forbes SA, et al. COSMIC: exploring the world's knowledge of somatic mutations in human cancer. Nucleic Acids Res 2015; 43:D805-D811.
85. Elhardt W, et al. Somatic cancer mutations in the DNMT2 tRNA methyltransferase alter its catalytic properties. Biochimie 2015; 112:66-72.
86. Schaefer M, et al. Azacytidine inhibits RNA methylation at DNMT2 target sites in human cancer cell lines. Cancer Res 2009; 69:8127-8132.
87. de Beus E, et al. Yeast NOP2 encodes an essential nucleolar protein with homology to a human proliferation marker. J Cell Biol 1994; 127 (6 Pt 2):1799-1813.
88. GustafsonWC, et al. Nucleolar protein p120 contains an arginine-rich domain that binds to ribosomal RNA. Biochem J 1998; 331 (Pt 2):387-393.
89. Freeman JW, et al. Identification and characterization of a human proliferationassociated nucleolar antigen with a molecular weight of 120,000 expressed in early G1 phase. Cancer Res 1988; 48:1244-1251.
90. Ochs RL, et al. Intranucleolar localization of human proliferating cell nucleolar antigen p120. Cancer Res 1988; 48:6523-6529.
91. Perlaky L, et al. Increased growth of NIH/3T3 cells by transfection with human p120 complementary DNA and inhibition by a p120 antisense construct. Cancer Res 1992; 52:428-436.
92. Frye M, Watt FM. The RNA methyltransferase Misu (NSun2) mediates Mycinduced proliferation and is upregulated in tumors. Curr Biol 2006; 16:971-981.
93. Frye M, et al. Genomic gain of 5p15 leads to over-expression of Misu (NSUN2) in breast cancer. Cancer Lett 2009.
94. Schmidt EV. The role of c-myc in regulation of translation initiation. Oncogene 2004; 23:3217-3221.
95. van Riggelen J, Yetil A, Felsher DW. MYC as a regulator of ribosome biogenesis and protein synthesis. Nat Rev Cancer 2010; 10:301-309.
96. Bartlett JM, et al. Mammostrat as a tool to stratify breast cancer patients at risk of recurrence during endocrine therapy. Breast Cancer Res 2010; 12:R47.