Pseudouridine in the anticodon of Escherichia coli tRNATyr(QΨA) is catalyzed by the dual specificity enzyme RluF

Journal of Biological Chemistry

Volumn 291, Issue 42, 2016, Pages 22327-22337

  Addepalli, Balasubrahmanyam ^a   Limbach, Patrick A ^a  

^a UNIVERSITY OF CINCINNATI   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACIDS; BIOSYNTHESIS; CHEMICAL DETECTION; CHROMATOGRAPHY; ENZYMES; GAS CHROMATOGRAPHY; LIQUID CHROMATOGRAPHY; MASS SPECTROMETRY; NUCLEIC ACIDS; RNA;

BACTERIAL EXPRESSION SYSTEMS; CHEMICAL DERIVATIZATION; GAS-PHASE DISSOCIATION; KNOCKOUT MUTANT; LIQUID CHROMATOGRAPHY TANDEM MASS SPECTROMETRY (LC MS/MS); MULTIPLE CHARACTERISTICS; MULTIPLE DETECTION; PROTEIN SYNTHESIS;

ESCHERICHIA COLI;

LUCIFERASE; MESSENGER RNA; PSEUDOURIDINE; RLUF SYNTHASE; SYNTHETASE; TYROSINE; TYROSINE TRANSFER RNA; UNCLASSIFIED DRUG; BACTERIAL RNA; ESCHERICHIA COLI PROTEIN; HYDROLYASE; PSEUDOURIDYLATE SYNTHETASE;

ANTICODON; ARTICLE; CONTROLLED STUDY; DERIVATIZATION; DISSOCIATION; ENZYME MECHANISM; ENZYME SPECIFICITY; ESCHERICHIA COLI; GENE EXPRESSION SYSTEM; GENE SEQUENCE; LIQUID CHROMATOGRAPHY; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN MODIFICATION; REPORTER GENE; RNA ANALYSIS; RNA TRANSLATION; TANDEM MASS SPECTROMETRY; CATALYSIS; GENE SILENCING; GENETICS; METABOLISM;

CATALYSIS; ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; GENE KNOCKDOWN TECHNIQUES; HYDRO-LYASES; PSEUDOURIDINE; RNA, BACTERIAL; RNA, TRANSFER, TYR;

EID: 84991777356     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M116.747865     Document Type: Article

References (63)

1. Machnicka, M. A., Milanowska, K., Osman Oglou, O., Purta, E., Kurkowska, M., Olchowik, A., Januszewski, W., Kalinowski, S., Dunin-Horkawicz, S., Rother, K. M., Helm, M., Bujnicki, J. M., and Grosjean, H. (2013) MODOMICS: a database of RNA modification pathways-2013 update. Nucleic Acids Res. 41, D262-D267
2. Limbach, P. A., Crain, P. F., and McCloskey, J. A. (1994) Summary: the modified nucleosides of RNA. Nucleic Acids Res. 22, 2183-2196
3. Cohn, W. E., and Volkin, E. (1951) Nucleoside-5′-phosphates from ribonucleic acid. Nature 167, 483-484
4. Spenkuch, F., Motorin, Y., and Helm, M. (2014) Pseudouridine: still mysterious, but never a fake (uridine)! RNA Biol. 11, 1540-1554
5. Charette, M., and Gray, M. W. (2000) Pseudouridine in RNA: what, where, how, and why. IUBMB Life 49, 341-351
6. Davis, D. R., Veltri, C. A., and Nielsen, L. (1998) An RNA model system for investigation of pseudouridine stabilization of the codon-anticodon interaction in tRNALys, tRNAHis and tRNATyr. J. Biomol. Struct. Dyn. 15, 1121-1132
7. Cunningham, P. R., Richard, R. B., Weitzmann, C. J., Nurse, K., and Ofengand, J. (1991) The absence of modified nucleotides affects both in vitro assembly and in vivo function of the 30S ribosomal subunit of Escherichia coli. Biochimie 73, 789-796
8. Yang, C., McPheeters, D. S., and Yu, Y. T. (2005) Ψ35 in the branch site recognition region of U2 small nuclear RNA is important for pre-mRNA splicing in Saccharomyces cerevisiae. J. Biol. Chem. 280, 6655-6662
9. Boros, G., Miko, E., Muramatsu, H., Weissman, D., Emri, E., Rózsa, D., Nagy, G., Juhász, A., Juhász, I., Van Der Horst, G., Horkay, I., Remenyik, É., Karikó, K., and Emri, G. (2013) Transfection of pseudouridine-modified mRNA encoding CPD-photolyase leads to repair of DNA damage in human keratinocytes: A new approach with future therapeutic potential. J. Photochem. Photobiol. B Biol. 129, 93-99
10. Hamma, T., and Ferré-D'Amaré, A. R. (2006) Pseudouridine synthases. Chem. Biol. 13, 1125-1135
11. Spedaliere, C. J., Ginter, J. M., Johnston, M. V., and Mueller, E. G. (2004) The pseudouridine synthases: revisiting a mechanism that seemed settled. J. Am. Chem. Soc. 126, 12758-12759
12. Hamma, T., and Ferré-D'Amaré, A. R. (2010) The box H/ACA ribonucleoprotein complex: interplay of RNA and protein structures in posttranscriptional RNA modification. J. Biol. Chem. 285, 805-809
13. McDonald, M. K., Miracco, E. J., Chen, J., Xie, Y., and Mueller, E. G. (2011) The handling of the mechanistic probe 5-fluorouridine by the pseudouridine synthase TruA and its consistency with the handling of the same probe by the pseudouridine synthases TruB and RluA. Biochemistry 50, 426-436
14. McCleverty, C. J., Hornsby, M., Spraggon, G., and Kreusch, A. (2007) Crystal structure of human Pus10, a novel pseudouridine synthase. J. Mol. Biol. 373, 1243-1254
15. Friedt, J., Leavens, F. M., Mercier, E., Wieden, H. J., and Kothe, U. (2014) An arginine-aspartate network in the active site of bacterial TruB is critical for catalyzing pseudouridine formation. Nucleic Acids Res. 42, 3857-3870
16. Ramamurthy, V., Swann, S. L., Paulson, J. L., Spedaliere, C. J., and Mueller, E. G. (1999) Critical aspartic acid residues in pseudouridine synthases. J. Biol. Chem. 274, 22225-22230
17. Conrad, J., Niu, L., Rudd, K., Lane, B. G., and Ofengand, J. (1999) 16S ribosomal RNApseudouridine synthase RsuA of Escherichia coli: deletion, mutation of the conserved Asp102 residue, and sequence comparison among all other pseudouridine synthases. RNA 5, 751-763
18. Gutgsell, N., Englund, N., Niu, L., Kaya, Y., Lane, B. G., and Ofengand, J. (2000) Deletion of the Escherichia coli pseudouridine synthase gene truB blocks formation of pseudouridine 55 in tRNA in vivo, does not affect exponential growth, but confers a strong selective disadvantage in competition with wild-type cells. RNA 6, 1870-1881
19. Raychaudhuri, S., Niu, L., Conrad, J., Lane, B. G., and Ofengand, J. (1999) Functional effect of deletion and mutation of the Escherichia coli ribosomal RNA and tRNA pseudouridine synthase RluA. J. Biol. Chem. 274, 18880-18886
20. Koonin, E. V. (1996) Pseudouridine synthases: four families of enzymes containing a putative uridine-binding motif also conserved in dUTPases and dCTP deaminases. Nucleic Acids Res. 24, 2411-2415
21. Kammen, H. O., Marvel, C. C., Hardy, L., and Penhoet, E. E. (1988) Purification, structure, and properties of Escherichia coli tRNA pseudouridine synthase I. J. Biol. Chem. 263, 2255-2263
22. Pomerantz, S. C., and McCloskey, J. A. (1990) Analysis of RNA hydrolyzates by liquid chromatography-mass spectrometry. Methods Enzymol. 193, 796-824
23. Ofengand, J., Del Campo, M., and Kaya, Y. (2001) Mapping pseudouridines in RNA molecules. Methods 25, 365-373
24. Carlile, T. M., Rojas-Duran, M. F., and Gilbert, W. V. (2015) Pseudo-Seq: genome-wide detection of pseudouridine modifications in RNA. Methods Enzymol. 560, 219-245
25. Carlile, T. M., Rojas-Duran, M. F., Zinshteyn, B., Shin, H., Bartoli, K. M., and Gilbert, W. V. (2014) Pseudouridine profiling reveals regulated mRNA pseudouridylation in yeast and human cells. Nature 515, 143-146
26. Durairaj, A., and Limbach, P. A. (2008) Mass spectrometry of the fifth nucleoside: a review of the identification of pseudouridine in nucleic acids. Anal. Chim. Acta 623, 117-125
27. Durairaj, A., and Limbach, P. A. (2008) Matrix-assisted laser desorption/ionization mass spectrometry screening for pseudouridine in mixtures of small RNAs by chemical derivatization, RNase digestion and signature products. Rapid Commun. Mass Spectrom. 22, 3727-3734
28. Durairaj, A., and Limbach, P. A. (2008) Improving CMC-derivatization of pseudouridine in RNA for mass spectrometric detection. Anal. Chim. Acta 612, 173-181
29. Patteson, K. G., Rodicio, L. P., and Limbach, P. A. (2001) Identification of the mass-silent post-transcriptionally modified nucleoside pseudouridine in RNA by matrix-assisted laser desorption/ionization mass spectrometry. Nucleic Acids Res. 29, E49-E49
30. Guymon, R., Pomerantz, S. C., Ison, J. N., Crain, P. F., and McCloskey, J. A. (2007) Post-transcriptional modifications in the small subunit ribosomal RNA from Thermotoga maritima, including presence of a novel modified cytidine. RNA 13, 396-403
31. Mengel-Jørgensen, J., and Kirpekar, F. (2002) Detection of pseudouridine and other modifications in tRNA by cyanoethylation and MALDI mass spectrometry. Nucleic Acids Res. 30, e135/131-e135/137
32. Pomerantz, S. C., and McCloskey, J. A. (2005) Detection of the common RNA nucleoside pseudouridine in mixtures of oligonucleotides by mass spectrometry. Anal. Chem. 77, 4687-4697
33. Addepalli, B., and Limbach, P. (2011) Mass spectrometry-based quantification of pseudouridine in RNA. J. Am. Soc. Mass Spectrom. 22, 1363-1372
34. Zhao, X., and Yu, Y.-T. (2004) Detection and quantitation of RNA base modifications. RNA 10, 996-1002
35. 6-methyladenosine. Nucleic Acids Res. 35, 6322-6329
36. Taucher, M., Ganisl, B., and Breuker, K. (2011) Identification, localization, and relative quantitation of pseudouridine in RNA by tandem mass spectrometry of hydrolysis products. Int. J. Mass Spectrom. 304, 91-97
37. Popova, A. M., and Williamson, J. R. (2014) Quantitative analysis of rRNA modifications using stable isotope labeling and mass spectrometry. J. Am. Chem. Soc. 136, 2058-2069
38. Goodman, H. M., Abelson, J. N., Landy, A., Zadrazil, S., and Smith, J. D. (1970) The nucleotide sequences of tyrosine transfer RNAs of Escherichia coli. Eur. J. Biochem. 13, 461-483
39. Del Campo, M., Kaya, Y., and Ofengand, J. (2001) Identification and site of action of the remaining four putative pseudouridine synthases in Escherichia coli. RNA 7, 1603-1615
40. Krivos, K. L., Addepalli, B., and Limbach, P. A. (2011) Removal of 3′- phosphate group by bacterial alkaline phosphatase improves oligonucleotide sequence coverage of RNase digestion products analyzed by collision-induced dissociation mass spectrometry. Rapid Commun. Mass Spectrom. 25, 3609-3616
41. Hossain, M., and Limbach, P. A. (2007) Mass spectrometry-based detection of transfer RNAs by their signature endonuclease digestion products. RNA 13, 295-303
42. Houser, W. M., Butterer, A., Addepalli, B., and Limbach, P. A. (2015) Combining recombinant ribonuclease U2 and protein phosphatase for RNA modification mapping by liquid chromatography-mass spectrometry. Anal. Biochem. 478, 52-58
43. Hur, S., and Stroud, R. M. (2007) How U38, 39, and 40 of many tRNAs become the targets for pseudouridylation by TruA. Mol. Cell 26, 189-203
44. Alian, A., DeGiovanni, A., Griner, S. L., Finer-Moore, J. S., and Stroud, R. M. (2009) Crystal structure of an RluF-RNA complex: a base-pair rearrangement is the key to selectivity of RluF for U2604 of the ribosome. J. Mol. Biol. 388, 785-800
45. Huang, L., Pookanjanatavip, M., Gu, X., and Santi, D. V. (1998) A conserved aspartate of tRNA pseudouridine synthase is essential for activity and a probable nucleophilic catalyst. Biochemistry 37, 344-351
46. Wrzesinski, J., Nurse, K., Bakin, A., Lane, B. G., and Ofengand, J. (1995) A dual-specificity pseudouridine synthase: an Escherichia coli synthase purified and cloned on the basis of its specificity for Ψ746 in 23S RNA is also specific for Ψ32 in tRNA(Phe). RNA 1, 437-448
47. Czudnochowski, N., Ashley, G. W., Santi, D. V., Alian, A., Finer-Moore, J., and Stroud, R. M. (2014) The mechanism of pseudouridine synthases from a covalent complex with RNA, and alternate specificity for U2605 versus U2604 between close homologs. Nucleic Acids Res. 42, 2037-2048
48. Hoang, C., and Ferré-D'Amaré, A. R. (2001) Cocrystal structure of a tRNA Ψ55 pseudouridine synthase: nucleotide flipping by an RNA-modifying enzyme. Cell 107, 929-939
49. Szweykowska-Kulinska, Z., and Beier, H. (1992) Sequence and structure requirements for the biosynthesis of pseudouridine (psi 35) in plant pretRNA(Tyr). EMBO J. 11, 1907-1912
50. Grosjean, H., Szweykowska-Kulinska, Z., Motorin, Y., Fasiolo, F., and Simos, G. (1997) Intron-dependent enzymatic formation of modified nucleosides in eukaryotic tRNAs: a review. Biochimie 79, 293-302
51. Kierzek, E., Malgowska, M., Lisowiec, J., Turner, D. H., Gdaniec, Z., and Kierzek, R. (2014) The contribution of pseudouridine to stabilities and structure of RNAs. Nucleic Acids Res. 42, 3492-3501
52. Bare, L. A., and Uhlenbeck, O. C. (1986) Specific substitution into the anticodon loop of yeast tyrosine transfer RNA. Biochemistry 25, 5825-5830
53. Davis, D. R. (1995) Stabilization of RNA stacking by pseudouridine. Nucleic Acids Res. 23, 5020-5026
54. Zerfass, K., and Beier, H. (1992) Pseudouridine in the anticodon GΨA of plant cytoplasmic tRNA(Tyr) is required for UAG and UAA suppression in the TMV-specific context. Nucleic Acids Res. 20, 5911-5918
55. 18O labeling and mass spectrometry. Anal. Chem. 77, 1891-1895
56. Li, M. M., Addepalli, B., Tu, M. J., Chen, Q. X., Wang, W. P., Limbach, P. A., LaSalle, J. M., Zeng, S., Huang, M., and Yu, A. M. (2015) Chimeric microRNA-1291 biosynthesized efficiently in Escherichia coli is effective to reduce target gene expression in human carcinoma cells and improve chemosensitivity. Drug Metab. Dispos. 43, 1129-1136
57. Wang, W. P., Ho, P. Y., Chen, Q. X., Addepalli, B., Limbach, P. A., Li, M. M., Wu, W. J., Jilek, J. L., Qiu, J. X., Zhang, H. J., Li, T., Wun, T., White, R. D., Lam, K. S., and Yu, A. M. (2015) Bioengineering novel chimeric microRNA-34a for prodrug cancer therapy: high-yield expression and purification, and structural and functional characterization. J. Pharmacol. Exp. Ther. 354, 131-141
58. Russell, S. P., and Limbach, P. A. (2013) Evaluating the reproducibility of quantifying modified nucleosides from ribonucleic acids by LC-UV-MS. J. Chromatogr. B Analyt. Technol. Biomed. Life Sci. 923-924, 74-82
59. Lee, C., Kramer, G., Graham, D. E., and Appling, D. R. (2007) Yeast mitochondrial initiator tRNA is methylated at guanosine 37 by the Trm5-encoded tRNA (guanine-N1-)-methyltransferase. J. Biol. Chem. 282, 27744-27753
60. Meeks, L. R., Addepalli, B., and Hunt, A. G. (2009) Characterization of genes encoding poly(A) polymerases in plants: evidence for duplication and functional specialization. PLoS One 4, e8082
61. Addepalli, B., Lesner, N. P., and Limbach, P. A. (2015) Detection of RNA nucleoside modifications with the uridine-specific ribonuclease MC1 from Momordica charantia. RNA 21, 1746-1756
62. Addepalli, B., and Hunt, A. G. (2007) A novel endonuclease activity associated with the Arabidopsis ortholog of the 30-kDa subunit of cleavage and polyadenylation specificity factor. Nucleic Acids Res. 35, 4453-4463
63. Kramer, E. B., and Farabaugh, P. J. (2007) The frequency of translational misreading errors in E. coli is largely determined by tRNA competition. RNA 13, 87-96