Different sensitivity of H69 modification enzymes RluD and RlmH to mutations in Escherichia coli 23S rRNA

Biochimie

Volumn 94, Issue 5, 2012, Pages 1080-1089

  Leppik, Margus ^a   Ero, Rya ^a   Liiv, Aivar ^a   Kipper, Kalle ^a   Remme, Jaanus ^a  

^a UNIVERSITY OF TARTU   (Estonia)

Author keywords

23S rRNA; Methylation; Pseudouridine; RlmH; RluD; Stem loop 69

Indexed keywords

NUCLEOSIDE; PSEUDOURIDINE; RLMH; RLUD; RNA 23S; SYNTHETASE; UNCLASSIFIED DRUG;

ARTICLE; CONTROLLED STUDY; ENZYME SPECIFICITY; ENZYME SUBSTRATE; ESCHERICHIA COLI; GENE; IN VITRO STUDY; METHYLATION; NONHUMAN; POINT MUTATION; PROTEIN MODIFICATION; RIBOSOME; RLMH GENE; RLUD GENE;

ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; HYDRO-LYASES; METHYLTRANSFERASES; MUTATION; PSEUDOURIDINE; RNA, RIBOSOMAL, 23S; SUBSTRATE SPECIFICITY;

ESCHERICHIA COLI;

EID: 84859424370     PISSN: 03009084     EISSN: 61831638     Source Type: Journal    
DOI: 10.1016/j.biochi.2012.02.023     Document Type: Article

References (63)

1. J. Ofengand, and M. Del Campo Modified Nucleosides in Escherichia coli Ribosomal RNA EcoSal - Escherichia Coli and Salmonella: Cellular and Molecular Biology 2004 ASM Press Washington chap. 4.6.1
2. W.A. Decatur, and M.J. Fournier rRNA modifications and ribosome function Trends Biochem. Sci. 27 2002 344 351
3. J. Ofengand Ribosomal RNA pseudouridines and pseudouridine synthases FEBS Lett. 514 2002 17 25
4. D.N. Wilson, and K.H. Nierhaus The weird and wonderful world of bacterial ribosome regulation Crit. Rev. Biochem. Mol. Biol. 42 2007 187 219
5. M. Del Campo, C. Recinos, G. Yanez, S.C. Pomerantz, R. Guymon, P.F. Crain, J.A. McCloskey, and J. Ofengand Number, position, and significance of the pseudouridines in the large subunit ribosomal RNA of Haloarcula marismortui and Deinococcus radiodurans RNA 2005 210 219
6. M. Kaczanowska, and M. Ryden-Aulin Ribosome biogenesis and the translation process in Escherichia coli Microbiol. Mol. Biol. Rev. 71 2007 477 494
7. Z. Xu, H.C. O'Farrell, J.P. Rife, and G.M. Culver A conserved rRNA methyltransferase regulates ribosome biogenesis Nat. Struct. Mol. Biol. 15 2008 534 536
8. P. Mitchell, M. Osswald, and R. Brimacombe Identification of intermolecular RNA cross-links at the subunit interface of the Escherichia coli ribosome Biochemistry 31 1992 3004 3011
9. M.M. Yusupov, G.Z. Yusupova, A. Baucom, K. Lieberman, T.N. Earnest, J.H. Cate, and H.F. Noller Crystal structure of the ribosome at 5.5 resolution Science 2001 883 896
10. B.S. Schuwirth, M.A. Borovinskaya, C.W. Hau, W. Zhang, A. Vila-Sanjurjo, J.M. Holton, and J.H. Cate Structures of the bacterial ribosome at 3.5 resolution Science 2005 827 834
11. R.K. Agrawal, C.M. Spahn, P. Penczek, R.A. Grassucci, K.H. Nierhaus, and J. Frank Visualization of tRNA movements on the Escherichia coli 70S ribosome during the elongation cycle J. Cell Biol. 150 2000 447 460
12. B.P. Klaholz, T. Pape, A.V. Zavialov, A.G. Myasnikov, E.V. Orlova, B. Vestergaard, M. Ehrenberg, and M. van Heel Structure of the Escherichia coli ribosomal termination complex with release factor 2 Nature 421 2003 90 94
13. B.P. Klaholz, A.G. Myasnikov, and M. van Heel Visualization of release factor 3 on the ribosome during termination of protein synthesis Nature 427 2004 862 865
14. R.K. Agrawal, M.R. Sharma, M.C. Kiel, G. Hirokawa, T.M. Booth, C.M. Spahn, R.A. Grassucci, A. Kaji, and J. Frank Visualization of ribosome-recycling factor on the Escherichia coli 70S ribosome: functional implications PNAS 101 2004 8900 8905
15. G.S. Allen, A. Zavialov, R. Gursky, M. Ehrenberg, and J. Frank The cryo-EM structure of a translation initiation complex from Escherichia coli Cell 121 2005 703 712
16. D.N. Wilson, F. Schluenzen, J.M. Harms, T. Yoshida, T. Ohkubo, R. Albrecht, J. Buerger, Y. Kobayashi, and P. Fucini X-ray crystallography study on ribosome recycling: the mechanism of binding and action of RRF on the 50S ribosomal subunit EMBO J. 24 2005 251 260
17. I.K. Ali, L. Lancaster, J. Feinberg, S. Joseph, and H.F. Noller Deletion of a conserved, central ribosomal intersubunit RNA bridge Mol. Cell 23 2006 865 874
18. N. Hirabayashi, N.S. Sato, and T. Suzuki Conserved loop sequence of helix 69 in Escherichia coli 23 S rRNA is involved in A-site tRNA binding and translational fidelity J. Biol. Chem. 281 2006 17203 17211
19. M. Selmer, C.M. Dunham, F.V.T. Murphy, A. Weixlbaumer, S. Petry, A.C. Kelley, J.R. Weir, and V. Ramakrishnan Structure of the 70S ribosome complexed with mRNA and tRNA Science 2006 1935 1942
20. R.D. Pai, W. Zhang, B.S. Schuwirth, G. Hirokawa, H. Kaji, A. Kaji, and J.H. Cate Structural insights into ribosome recycling factor interactions with the 70S ribosome J. Mol. Biol. 376 2008 1334 1347
21. U. Rawat, H. Gao, A. Zavialov, R. Gursky, M. Ehrenberg, and J. Frank Interactions of the release factor RF1 with the ribosome as revealed by cryo-EM J. Mol. Biol. 357 2006 1144 1153
22. A. Korostelev, H. Asahara, L. Lancaster, M. Laurberg, A. Hirschi, J. Zhu, S. Trakhanov, W.G. Scott, and H.F. Noller Crystal structure of a translation termination complex formed with release factor RF2 PNAS 105 2008 19684 19689
23. A. Weixlbaumer, H. Jin, C. Neubauer, R.M. Voorhees, S. Petry, A.C. Kelley, and V. Ramakrishnan Insights into translational termination from the structure of RF2 bound to the ribosome Science 2008 953 956
24. M. Laurberg, H. Asahara, A. Korostelev, J. Zhu, S. Trakhanov, and H.F. Noller Structural basis for translation termination on the 70S ribosome Nature 454 2008 852 857
25. Y. Sakakibara, and C.S. Chow Probing conformational states of modified helix 69 in 50S ribosomes J. Am. Chem. Soc. 133 2011 8396 8399
26. J. Harms, F. Schluenzen, R. Zarivach, A. Bashan, S. Gat, I. Agmon, H. Bartels, F. Franceschi, and A. Yonath High resolution structure of the large ribosomal subunit from a mesophilic eubacterium Cell 107 2001 679 688
27. M. O'Connor, and A.E. Dahlberg The involvement of two distinct regions of 23 S ribosomal RNA in tRNA selection J. Mol. Biol. 254 1995 838 847
28. U. Maiväli, and J. Remme Definition of bases in 23S rRNA essential for ribosomal subunit association RNA 2004 600 604
29. A. Liiv, D. Karitkina, U. Maiväli, and J. Remme Analysis of the function of E. coli 23S rRNA helix-loop 69 by mutagenesis BMC Mol. Biol. 6 2005 18
30. K. Kipper, C. Hetenyi, S. Sild, J. Remme, and A. Liiv Ribosomal intersubunit bridge B2a is involved in factor-dependent translation initiation and translational processivity J. Mol. Biol. 385 2009 405 422
31. M. O'Connor Helix 69 in 23S rRNA modulates decoding by wild type and suppressor tRNAs Mol. Genet. Genomics 282 2009 371 380
32. A. Bakin, and J. Ofengand Four newly located pseudouridylate residues in Escherichia coli 23S ribosomal RNA are all at the peptidyltransferase center: analysis by the application of a new sequencing technique Biochemistry 32 1993 9754 9762
33. J.A. Kowalak, E. Bruenger, T. Hashizume, J.M. Peltier, J. Ofengand, and J.A. McCloskey Structural characterization of U*-1915 in domain IV from Escherichia coli 23S ribosomal RNA as 3-methylpseudouridine Nucleic Acids Res. 24 1996 688 693
34. M. Meroueh, P.J. Grohar, J. Qiu, J. SantaLucia Jr., S.A. Scaringe, and C.S. Chow Unique structural and stabilizing roles for the individual pseudouridine residues in the 1920 region of Escherichia coli 23S rRNA Nucleic Acids Res. 28 2000 2075 2083
35. J.P. Desaulniers, Y.C. Chang, R. Aduri, S.C. Abeysirigunawardena, J. SantaLucia Jr., and C.S. Chow Pseudouridines in rRNA helix 69 play a role in loop stacking interactions Org. Biomol. Chem. 6 2008 3892 3895
36. H.M. Chui, M. Meroueh, S.A. Scaringe, and C.S. Chow Synthesis of a 3-methyluridine phosphoramidite to investigate the role of methylation in a ribosomal RNA hairpin Bioorg. Med. Chem. 10 2002 325 332
37. H.M. Chui, J.P. Desaulniers, S.A. Scaringe, and C.S. Chow Synthesis of helix 69 of Escherichia coli 23S rRNA containing its natural modified nucleosides, m(3)Psi and Psi J. Org. Chem. 67 2002 8847 8854
38. K. Kipper, S. Sild, C. Hetenyi, J. Remme, and A. Liiv Pseudouridylation of 23S rRNA helix 69 promotes peptide release by release factor RF2 but not by release factor RF1 Biochimie 93 2011 834 844
39. M. Ejby, M.A. Sorensen, and S. Pedersen Pseudouridylation of helix 69 of 23S rRNA is necessary for an effective translation termination PNAS 104 2007 19410 19415
40. N.S. Gutgsell, M.P. Deutscher, and J. Ofengand The pseudouridine synthase RluD is required for normal ribosome assembly and function in Escherichia coli RNA 2005 1141 1152
41. J. Conrad, D. Sun, N. Englund, and J. Ofengand The rluC gene of Escherichia coli codes for a pseudouridine synthase that is solely responsible for synthesis of pseudouridine at positions 955, 2504, and 2580 in 23 S ribosomal RNA J. Biol. Chem. 273 1998 18562 18566
42. L. Huang, J. Ku, M. Pookanjanatavip, X. Gu, D. Wang, P.J. Greene, and D.V. Santi Identification of two Escherichia coli pseudouridine synthases that show multisite specificity for 23S RNA Biochemistry 37 1998 15951 15957
43. J. Wrzesinski, K. Nurse, A. Bakin, B.G. Lane, and J. Ofengand A dual-specificity pseudouridine synthase: an Escherichia coli synthase purified and cloned on the basis of its specificity for psi 746 in 23S RNA is also specific for psi 32 in tRNA(phe) RNA 1995 437 448
44. T. Siibak, and J. Remme Subribosomal particle analysis reveals the stages of bacterial ribosome assembly at which rRNA nucleotides are modified RNA 2010 2023 2032
45. G.R. Björk Biosynthesis and function of modified nucleosides D. Söll, U.L. Rajbhandary, tRNA: Structure, Biosynthesis, and Function 1995 165 205
46. J. Ofengand, A. Malhotra, J. Remme, N.S. Gutgsell, M. Del Campo, S. Jean-Charles, L. Peil, and Y. Kaya Pseudouridines and pseudouridine synthases of the ribosome Cold Spring Harbor Symposia Quantitative Biol. 66 2001 147 159
47. S. Raychaudhuri, J. Conrad, B.G. Hall, and J. Ofengand A pseudouridine synthase required for the formation of two universally conserved pseudouridines in ribosomal RNA is essential for normal growth of Escherichia coli RNA 1998 1407 1417
48. P.P. Vaidyanathan, M.P. Deutscher, and A. Malhotra RluD, a highly conserved pseudouridine synthase, modifies 50S subunits more specifically and efficiently than free 23S rRNA RNA 2007 1868 1876
49. M. Leppik, L. Peil, K. Kipper, A. Liiv, and J. Remme Substrate specificity of the pseudouridine synthase RluD in Escherichia coli FEBS J. 274 2007 5759 5766
50. R. Ero, M. Leppik, A. Liiv, and J. Remme Specificity and kinetics of 23S rRNA modification enzymes RlmH and RluD RNA 2010 2075 2084
51. R. Ero, L. Peil, A. Liiv, and J. Remme Identification of pseudouridine methyltransferase in Escherichia coli RNA 2008 2223 2233
52. E. Purta, K.H. Kaminska, J.M. Kasprzak, J.M. Bujnicki, and S. Douthwaite YbeA is the m3Psi methyltransferase RlmH that targets nucleotide 1915 in 23S rRNA RNA 2008 2234 2244
53. J. Armistead, S. Khatkar, B. Meyer, B.L. Mark, N. Patel, G. Coghlan, R.E. Lamont, S. Liu, J. Wiechert, P.A. Cattini, P. Koetter, K. Wrogemann, C.R. Greenberg, K.D. Entian, T. Zelinski, and B. Triggs-Raine Mutation of a gene essential for ribosome biogenesis, EMG1, causes Bowen-Conradi syndrome Am. J. Hum. Genet. 84 2009 728 739
54. J.P. Wurm, B. Meyer, U. Bahr, M. Held, O. Frolow, P. Kotter, J.W. Engels, A. Heckel, M. Karas, K.D. Entian, and J. Wohnert The ribosome assembly factor Nep1 responsible for Bowen-Conradi syndrome is a pseudouridine-N1-specific methyltransferase Nucleic Acids Res. 38 2010 2387 2398
55. F.R. Blattner, G. Plunkett 3rd, C.A. Bloch, N.T. Perna, V. Burland, M. Riley, J. Collado-Vides, J.D. Glasner, C.K. Rode, G.F. Mayhew, J. Gregor, N.W. Davis, H.A. Kirkpatrick, M.A. Goeden, D.J. Rose, B. Mau, and Y. Shao The complete genome sequence of Escherichia coli K-12 Science 1997 1453 1462
56. A.A. Leonov, P.V. Sergiev, A.A. Bogdanov, R. Brimacombe, and O.A. Dontsova Affinity purification of ribosomes with a lethal G2655C mutation in 23 S rRNA that affects the translocation J. Biol. Chem. 278 2003 25664 25670
57. J. Ofengand, M. Del Campo, and Y. Kaya Mapping pseudouridines in RNA molecules Methods 2001 365 373
58. A. Liiv, and M. O'Connor Mutations in the intersubunit bridge regions of 23 S rRNA J. Biol. Chem. 281 2006 29850 29862
59. T.T. Lee, S. Agarwalla, and R.M. Stroud A unique RNA fold in the RumA-RNA-cofactor ternary complex contributes to substrate selectivity and enzymatic function Cell 120 2005 599 611
60. C. Hoang, and A.R. Ferre-D'Amare Cocrystal structure of a tRNA Psi55 pseudouridine synthase: nucleotide flipping by an RNA-modifying enzyme Cell 107 2001 929 939
61. C. Hoang, J. Chen, C.A. Vizthum, J.M. Kandel, C.S. Hamilton, E.G. Mueller, and A.R. Ferre-D'Amare Crystal structure of pseudouridine synthase RluA: indirect sequence readout through protein-induced RNA structure Mol. Cell 24 2006 535 545
62. Modomics http://modomics.genesilico.pl/.
63. RNA Modification database http://rna-mdb.cas.albany.edu/RNAmods/.