From end to end: TRNA editing at 5′-and 3′-terminal positions

International Journal of Molecular Sciences

Volumn 15, Issue 12, 2014, Pages 23975-23998

  Betat, Heike ^a   Long, Yicheng ^b   Jackman, Jane E ^b   Mörl, Mario ^a  

^a UNIVERSITY OF LEIPZIG   (Germany)

^b OHIO STATE UNIVERSITY   (United States)

Author keywords

Editing; tRNA; tRNA maturation; tRNA processing

Indexed keywords

CYCLIC NUCLEOTIDE; DNA DIRECTED RNA POLYMERASE; NUCLEOSIDE; NUCLEOTIDYLTRANSFERASE; TRANSFER RNA;

ENZYME ACTIVITY; GENETIC HETEROGENEITY; GENETIC TRANSCRIPTION; GENOME ANALYSIS; HUMAN; MICROBIAL DIVERSITY; MITOCHONDRIAL GENETICS; NONHUMAN; POLYMERIZATION; REVIEW; RNA SEQUENCE; SEQUENCE ANALYSIS; ANIMAL; EVOLUTION; GENETICS; METABOLISM; RNA EDITING; SACCHAROMYCES CEREVISIAE;

ANIMALS; BIOLOGICAL EVOLUTION; HUMANS; RNA EDITING; RNA, TRANSFER; SACCHAROMYCES CEREVISIAE;

EID: 84919784553     PISSN: 16616596     EISSN: 14220067     Source Type: Journal    
DOI: 10.3390/ijms151223975     Document Type: Review

References (92)

1. Giegé, R.; Jühling, F.; Pütz, J.; Stadler, P.; Sauter, C.; Florentz, C. Structure of transfer RNAs: Similarity and variability. Wiley Interdiscip. Rev. 2012, 3, 37-61.
2. Phizicky, E.M.; Hopper, A.K. tRNA biology charges to the front. Genes Dev. 2010, 24, 1832-1860.
3. Paris, Z.; Fleming Ian, M.C.; Alfonzo, J.D. Determinants of tRNA editing and modification: Avoiding conundrums, affecting function. Semin. Cell Dev. Biol. 2012, 23, 269-274.
4. Jackman, J.E.; Alfonzo, J.D. Transfer RNA modifications: Nature’s combinatorial chemistry playground. Wiley Interdiscip. Rev. 2013, 4, 35-48.
5. Lohan, A.J.; Gray, M.W. Analysis of 5'-or 3'-terminal tRNA editing: Mitochondrial 5' tRNA editing in Acanthamoeba castellanii as the exemplar. Methods Enzymol. 2007, 424, 223-242.
6. Gray, M.W. Evolutionary origin of RNA editing. Biochemistry 2012, 51, 5235-5242.
7. Schuster, J.; Mörl, M. Mitochondrial tRNA editing. In Mitochondrial Function and Biogenesis; Springer Berlin Heidelberg: Berlin/Heidelberg, Germany, 2004; pp. 81-96.
8. Zhou, W.; Karcher, D.; Bock, R. Importance of adenosine-to-inosine editing adjacent to the anticodon in an Arabidopsis alanine tRNA under environmental stress. Nucleic Acids Res. 2013, 41, 3362-3372.
9. Zhou, W.; Karcher, D.; Bock, R. Identification of enzymes for adenosine-to-inosine editing and discovery of cytidine-to-uridine editing in nucleus-encoded tRNAs of Arabidopsis. Plant Physiol. 2014, 166, 1985-1997.
10. Randau, L.; Stanley, B.J.; Kohlway, A.; Mechta, S.; Xiong, Y.; Soll, D. A cytidine deaminase edits C to U in transfer RNAs in archaea. Science 2009, 324, 657-659.
11. Marechal-Drouard, L.; Kumar, R.; Remacle, C.; Small, I. RNA editing of larch mitochondrial tRNAHis precursors is a prerequisite for processing. Nucleic Acids Res. 1996, 24, 3229-3234.
12. Fey, J.; Weil, J.H.; Tomita, K.; Cosset, A.; Dietrich, A.; Small, I.; Marechal-Drouard, L. Role of editing in plant mitochondrial transfer RNAs. Gene 2002, 286, 21-24.
13. Price, D.H.; Gray, M.W. A novel nucleotide incorporation activity implicated in the editing of mitochondrial transfer RNAs in Acanthamoeba castellanii. RNA 1999, 5, 302-317.
14. Mörl, M.; Dörner, M.; Pääbo, S. C to U editing and modifications during the maturation of the mitochondrial tRNAAsp in marsupials. Nucleic Acids Res. 1995, 23, 3380-3384.
15. Lonergan, K.M.; Gray, M.W. Editing of transfer RNAs in Acanthamoeba castellanii mitochondria. Science 1993, 259, 812-816.
16. Lonergan, K.M.; Gray, M.W. Predicted editing of additional transfer RNAs in Acanthamoeba castellanii mitochondria. Nucleic Acids Res. 1993, 21, 4402.
17. Alfonzo, J.D.; Blanc, V.; Estevez, A.M.; Rubio, M.A.; Simpson, L. C to U editing of the anticodon of imported mitochondrial tRNATrp allows decoding of the UGA stop codon in Leishmania tarentolae. EMBO J. 1999, 18, 7056-7062.
18. Janke, A.; Paabo, S. Editing of a tRNA anticodon in marsupial mitochondria changes its codon recognition. Nucleic Acids Res. 1993, 21, 1523-1525.
19. Antes, T.; Costandy, H.; Mahendran, R.; Spottswood, M.; Miller, D. Insertional editing of mitochondrial tRNAs of Physarum polycephalum and Didymium nigripes. Mol. Cell. Biol. 1998, 18, 7521-7527.
20. Walker, S.C.; Engelke, D.R. Ribonuclease P: The evolution of an ancient RNA enzyme. Crit. Rev. Biochem. Mol. Biol. 2006, 41, 77-102.
21. Orellana, O.; Cooley, L.; Soll, D. The additional guanylate at the 5' terminus of Escherichia coli tRNAHis is the result of unusual processing by RNase P. Mol. Cell. Biol. 1986, 6, 525-529.
22. Burkard, U.; Soll, D. The 5'-terminal guanylate of chloroplast histidine tRNA is encoded in its gene. J. Biol. Chem. 1988, 263, 9578-9581.
23. Burkard, U.; Willis, I.; Soll, D. Processing of histidine transfer RNA precursors. Abnormal cleavage site for RNase P. J. Biol. Chem. 1988, 263, 2447-2451.
24. Kikovska, E.; Brannvall, M.; Kufel, J.; Kirsebom, L.A. Substrate discrimination in RNase P RNA-mediated cleavage: Importance of the structural environment of the RNase P cleavage site. Nucleic Acids Res. 2005, 33, 2012-2021.
25. Kufel, J.; Kirsebom, L.A. Different cleavage sites are aligned differently in the active site of M1 RNA, the catalytic subunit of Escherichia coli RNase P. Proc. Natl. Acad. Sci. USA 1996, 93, 6085-6090.
26. Chen, W.Y.; Singh, D.; Lai, L.B.; Stiffler, M.A.; Lai, H.D.; Foster, M.P.; Gopalan, V. Fidelity of tRNA 5'-maturation: A possible basis for the functional dependence of archaeal and eukaryal RNase P on multiple protein cofactors. Nucleic Acids Res. 2012, 40, 4666-4680.
27. Randau, L.; Schroder, I.; Soll, D. Life without RNase P. Nature 2008, 453, 120-123.
28. Li, Y.; Altman, S. In search of RNase P RNA from microbial genomes. RNA 2004, 10, 1533-1540.
29. Price, D.H.; Gray, M.W. Confirmation of predicted edits and demonstration of unpredicted edits in Acanthamoeba castellanii mitochondrial tRNAs. Curr. Genet. 1999, 35, 23-29.
30. Laforest, M.J.; Bullerwell, C.E.; Forget, L.; Lang, B.F. Origin, evolution, and mechanism of 5' tRNA editing in chytridiomycete fungi. RNA 2004, 10, 1191-1199.
31. Bullerwell, C.E. In vitro characterization of a tRNA editing activity in the mitochondria of Spizellomyces punctatus, a Chytridiomycete Fungus. J. Biol. Chem. 2004, 280, 2463-2470.
32. Gott, J.M.; Somerlot, B.H.; Gray, M.W. Two forms of RNA editing are required for tRNA maturation in Physarum mitochondria. RNA 2010, 16, 482-488.
33. Abad, M.G.; Long, Y.; Kinchen, R.D.; Schindel, E.T.; Gray, M.W.; Jackman, J.E. Mitochondrial tRNA 5'-editing in Dictyostelium discoideum and Polysphondylium pallidum. J. Biol. Chem. 2014, 289, 15155-15165.
34. Gu, W.; Hurto, R.L.; Hopper, A.K.; Grayhack, E.J.; Phizicky, E.M. Depletion of Saccharomyces cerevisiae tRNAHis guanylyltransferase Thg1p leads to uncharged tRNAHis with additional m5C. Mol. Cell. Biol. 2005, 25, 8191-8201.
35. Gu, W.; Jackman, J.E.; Lohan, A.J.; Gray, M.W.; Phizicky, E.M. tRNAHis maturation: An essential yeast protein catalyzes addition of a guanine nucleotide to the 5' end of tRNAHis. Genes Dev. 2003, 17, 2889-2901.
36. Jackman, J.E. tRNAHis guanylyltransferase catalyzes a 3'-5' polymerization reaction that is distinct from G-1 addition. Proc. Natl. Acad. Sci. USA 2006, 103, 8640-8645.
37. Smith, B.A.; Jackman, J.E. Kinetic analysis of 3'-5' nucleotide addition catalyzed by eukaryotic tRNAHis guanylyltransferase. Biochemistry 2012, 51, 453-465.
38. Smith, B.A.; Jackman, J.E. Saccharomyces cerevisiae Thg1 uses 5'-pyrophosphate removal to control addition of nucleotides to tRNAHis. Biochemistry 2014, 53, 1380-1391.
39. Jackman, J.E.; Gott, J.M.; Gray, M.W. Doing it in reverse: 3'-to-5' polymerization by the Thg1 superfamily. RNA 2012, 18, 886-899.
40. Abad, M.G.; Rao, B.S.; Jackman, J.E. Template-dependent 3'-5' nucleotide addition is a shared feature of tRNAHis guanylyltransferase enzymes from multiple domains of life. Proc. Natl. Acad. Sci. USA 2010, 107, 674-679.
41. Heinemann, I.U.; Randau, L.; Tomko, R.J., Jr.; Söll, D. 3'-5' tRNAHis guanylyltransferase in bacteria. FEBS Lett. 2010, 584, 3567-3572.
42. Rao, B.S.; Maris, E.L.; Jackman, J.E. tRNA 5'-end repair activities of tRNAHis guanylyltransferase (Thg1)-like proteins from bacteria and archaea. Nucleic Acids Res. 2011, 39, 1833-1842.
43. Abad, M.G.; Long, Y.; Willcox, A.; Gott, J.M.; Gray, M.W.; Jackman, J.E. A role for tRNAHis guanylyltransferase (Thg1)-like proteins from Dictyostelium discoideum in mitochondrial 5'-tRNA editing. RNA 2011, 17, 613-623.
44. Rao, B.S.; Mohammad, F.; Gray, M.W.; Jackman, J.E. Absence of a universal element for tRNAHis identity in Acanthamoeba castellanii. Nucleic Acids Res. 2013, 41, 1885-1894.
45. Yuan, Y.; Altman, S. Substrate recognition by human RNase P: Identification of small, model substrates for the enzyme. EMBO J. 1995, 14, 159-168.
46. Dewe, J.M.; Whipple, J.M.; Chernyakov, I.; Jaramillo, L.N.; Phizicky, E.M. The yeast rapid tRNA decay pathway competes with elongation factor 1A for substrate tRNAs and acts on tRNAs lacking one or more of several modifications. RNA 2012, 18, 1886-1896.
47. Whipple, J.M.; Lane, E.A.; Chernyakov, I.; D’Silva, S.; Phizicky, E.M. The yeast rapid tRNA decay pathway primarily monitors the structural integrity of the acceptor and T-stems of mature tRNA. Genes Dev. 2011, 25, 1173-1184.
48. Naganuma, M.; Sekine, S.; Chong, Y.E.; Guo, M.; Yang, X.L.; Gamper, H.; Hou, Y.M.; Schimmel, P.; Yokoyama, S. The selective tRNA aminoacylation mechanism based on a single G·U pair. Nature 2014, 510, 507-511.
49. Gabriel, K.; Schneider, J.; McClain, W.H. Functional evidence for indirect recognition of G·U in tRNAAla by alanyl-tRNA synthetase. Science 1996, 271, 195-197.
50. McClain, W.H.; Gabriel, K.; Schneider, J. Specific function of a G·U wobble pair from an adjacent helical site in tRNAAla during recognition by alanyl-tRNA synthetase. RNA 1996, 2, 105-109.
51. Lizano, E.; Scheibe, M.; Rammelt, C.; Betat, H.; Mörl, M. A comparative analysis of CCA-adding enzymes from human and E. coli: Differences in CCA addition and tRNA 3'-end repair. Biochimie 2008, 90, 762-772.
52. Zhu, L.; Deutscher, M.P. tRNA nucleotidyltransferase is not essential for Escherichia coli viability. EMBO J. 1987, 6, 2473-2477.
53. Binder, S.; Marchfelder, A.; Brennicke, A. RNA editing of tRNAPhe and tRNACys in mitochondria of Oenothera berteriana is initiated in precursor molecules. Mol. Gen. Genet. 1994, 244, 67-74.
54. Marechal-Drouard, L.; Cosset, A.; Remacle, C.; Ramamonjisoa, D.; Dietrich, A. A single editing event is a prerequisite for efficient processing of potato mitochondrial phenylalanine tRNA. Mol. Cell. Biol. 1996, 16, 3504-3510.
55. Himeno, H.; Hasegawa, T.; Ueda, T.; Watanabe, K.; Miura, K.; Shimizu, M. Role of the extra G-C pair at the end of the acceptor stem of tRNAHis in aminoacylation. Nucleic Acids Res. 1989, 17, 7855-7863.
56. Nameki, N.; Asahara, H.; Shimizu, M.; Okada, N.; Himeno, H. Identity elements of Saccharomyces cerevisiae tRNAHis. Nucleic Acids Res. 1995, 23, 389-394.
57. Rosen, A.E.; Musier-Forsyth, K. Recognition of G-1: C73 atomic groups by Escherichia coli histidyl-tRNA synthetase. J. Am. Chem. Soc. 2004, 126, 64-65.
58. Giege, R.; Sissler, M.; Florentz, C. Universal rules and idiosyncratic features in tRNA identity. Nucleic Acids Res. 1998, 26, 5017-5035.
59. Yan, W.; Francklyn, C. Cytosine 73 is a discriminator nucleotide in vivo for histidyl-tRNA in Escherichia coli. J. Biol. Chem. 1994, 269, 10022-10027.
60. Preston, M.A.; Phizicky, E.M. The requirement for the highly conserved G-1 residue of Saccharomyces cerevisiae tRNAHis can be circumvented by over-expression of tRNAHis and its synthetase. RNA 2010, 16, 1068-1077.
61. Cooley, L.; Appel, B.; Söll, D. Post-transcriptional nucleotide addition is responsible for the formation of the 5' terminus of histidine tRNA. Proc. Natl. Acad. Sci. USA 1982, 79, 6475-6479.
62. Wang, C.; Sobral, B.W.; Williams, K.P. Loss of a universal tRNA feature. J. Bacteriol. 2007, 189, 1954-1962.
63. Yuan, J.; Gogakos, T.; Babina, A.M.; Soll, D.; Randau, L. Change of tRNA identity leads to a divergent orthogonal histidyl-tRNA synthetase/tRNAHis pair. Nucleic Acids Res. 2011, 39, 2286-2293.
64. Ardell, D.H.; Andersson, S.G. TFAM detects co-evolution of tRNA identity rules with lateral transfer of histidyl-tRNA synthetase. Nucleic Acids Res. 2006, 34, 893-904.
65. Lavrov, D.V.; Brown, W.M.; Boore, J.L. A novel type of RNA editing occurs in the mitochondrial tRNAs of the centipede Lithobius forficatus. Proc. Natl. Acad. Sci. USA 2000, 97, 13738-13742.
66. Leigh, J.; Lang, B.F. Mitochondrial 3' tRNA editing in the jakobid Seculamonas ecuadoriensis: A novel mechanism and implications for tRNA processing. RNA 2004, 10, 615-621.
67. Reichert, A.; Rothbauer, U.; Morl, M. Processing and editing of overlapping tRNAs in human mitochondria. J. Biol. Chem. 1998, 273, 31977-31984.
68. Yokobori, S.; Paabo, S. Transfer RNA editing in land snail mitochondria. Proc. Natl. Acad. Sci. USA 1995, 92, 10432-10435.
69. Yokobori, S.; Paabo, S. Polyadenylation creates the discriminator nucleotide of chicken mitochondrial tRNATyr. J. Mol. Biol. 1997, 265, 95-99.
70. Yokobori, S.I.; Paabo, S. tRNA editing in metazoans. Nature 1995, 377, 490.
71. Kurland, C.G. Evolution of mitochondrial genomes and the genetic code. Bioessays 1992, 14, 709-714.
72. Tomita, K.; Ueda, T.; Watanabe, K. RNA editing in the acceptor stem of squid mitochondrial tRNATyr. Nucleic Acids Res. 1996, 24, 4987-4991.
73. Steinberg, S.; Misch, A.; Sprinzl, M. Compilation of tRNA sequences and sequences of tRNA genes. Nucleic. Acids Res. 1993, 21, 3011-3015.
74. Nagaike, T.; Suzuki, T.; Ueda, T. Polyadenylation in mammalian mitochondria: Insights from recent studies. Biochim. Biophys. Acta 2008, 1779, 266-269.
75. Chang, J.H.; Tong, L. Mitochondrial poly(A) polymerase and polyadenylation. Biochim. Biophys. Acta 2012, 1819, 992-997.
76. Rorbach, J.; Nicholls, T.J.; Minczuk, M. PDE12 removes mitochondrial RNA poly(A) tails and controls translation in human mitochondria. Nucleic Acids Res. 2011, 39, 7750-7763.
77. Reichert, A.S.; Mörl, M. Repair of tRNAs in metazoan mitochondria. Nucleic Acids Res. 2000, 28, 2043-2048.
78. Schuster, J.; Betat, H.; Morl, M. Is yeast on its way to evolving tRNA editing? EMBO Rep. 2005, 6, 367-372.
79. Hong, Y.; Cole, T.E.; Brasier, C.M.; Buck, K.W. Evolutionary relationships among putative RNA-dependent RNA polymerases encoded by a mitochondrial virus-like RNA in the Dutch Elm disease fungus, Ophiostoma novo-ulmi, by other viruses and virus-like RNAs and by the Arabidopsis mitochondrial genome. Virology 1998, 246, 158-169.
80. Scheffler, I.E. Mitochondria; Wiley-Liss: New York, NY, USA, 1999.
81. Li, Z.; Deutscher, M.P. The role of individual exoribonucleases in processing at the 3' end of Escherichia coli tRNA precursors. J. Biol. Chem. 1994, 269, 6064-6071.
82. Li, Z.; Deutscher, M.P. RNase E plays an essential role in the maturation of Escherichia coli tRNA precursors. RNA 2002, 8, 97-109.
83. Ow, M.C.; Kushner, S.R. Initiation of tRNA maturation by RNase E is essential for cell viability in E. coli. Genes Dev. 2002, 16, 1102-1115.
84. Jia, H.; Wang, X.; Liu, F.; Guenther, U.-P.; Srinivasan, S.; Anderson, J.T.; Jankowsky, E. The RNA helicase Mtr4p modulates polyadenylation in the TRAMP complex. Cell 2011, 145, 890-901.
85. Dickinson, H.; Tretbar, S.; Betat, H.; Morl, M. The TRAMP complex shows tRNA editing activity in S. cerevisiae. Mol. Biol. Evol. 2012, 29, 1451-1459.
86. LaCava, J.; Houseley, J.; Saveanu, C.; Petfalski, E.; Thompson, E.; Jacquier, A.; Tollervey, D. RNA degradation by the exosome is promoted by a nuclear polyadenylation complex. Cell 2005, 121, 713-724.
87. Vanácová, S.; Wolf, J.; Martin, G.; Blank, D.; Dettwiler, S.; Friedlein, A.; Langen, H.; Keith, G.; Keller, W. A new yeast poly(A) polymerase complex involved in RNA quality control. PLoS Biol. 2005, 3, e189.
88. Wyers, F.; Rougemaille, M.; Badis, G.; Rousselle, J.-C.; Dufour, M.-E.; Boulay, J.; Regnault, B.; Devaux, F.; Namane, A.; Seraphin, B., et al. Cryptic pol II transcripts are degraded by a nuclear quality control pathway involving a new poly(A) polymerase. Cell 2005, 121, 725-737.
89. Cavalier-Smith, T. Cell and genome coevolution: Facultative anaerobiosis, glycosomes and kinetoplastan RNA editing. Trends Genet. 1997, 13, 6-9.
90. Covello, P.S.; Gray, M.W. On the evolution of RNA editing. Trends Genet. 1993, 9, 265-268.
91. Khersonsky, O.; Tawfik, D.S. Enzyme promiscuity: A mechanistic and evolutionary perspective. Annu. Rev. Biochem. 2010, 79, 471-505.
92. Simpson, L.; Thiemann, O.H.; Savill, N.J.; Alfonzo, J.D.; Maslov, D.A. Evolution of RNA editing in trypanosome mitochondria. Proc. Natl. Acad. Sci. USA 2000, 97, 6986-6993.