Specificity and kinetics of 23S rRNA modification enzymes RlmH and RluD

RNA

Volumn 16, Issue 11, 2010, Pages 2075-2084

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

^a UNIVERSITY OF TARTU   (Estonia)

Author keywords

23S rRNA; Catalytic properties; Post transcriptional modification; Ribosome assembly; RlmH; RluD

Indexed keywords

PROTEIN RLMH; PROTEIN RLUD; PSEUDOURIDINE; RIBOSOME RNA; RNA 23S; S ADENOSYLMETHIONINE; SYNTHETASE; UNCLASSIFIED DRUG; URIDINE;

ARTICLE; ENZYME KINETICS; ENZYME SPECIFICITY; ESCHERICHIA COLI; METHYLATION; PRIORITY JOURNAL; RIBOSOME SUBUNIT; RNA PROCESSING;

ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; HYDRO-LYASES; KINETICS; METHYLATION; METHYLTRANSFERASES; RNA, RIBOSOMAL, 23S; SUBSTRATE SPECIFICITY;

ESCHERICHIA COLI;

EID: 78149292161     PISSN: 13558382     EISSN: 14699001     Source Type: Journal    
DOI: 10.1261/rna.2234310     Document Type: Article

References (53)

1. Agarwalla S, Kealey JT, Santi DV, Stroud RM. 2002. Characterization of the 23 S ribosomal RNA m5U1939 methyltransferase from Escherichia coli. J Biol Chem 277: 8835-8840. (Pubitemid 34952950)
2. Agrawal RK, Sharma MR, Kiel MC, Hirokawa G, Booth TM, Spahn CM, Grassucci RA, Kaji A, Frank J. 2004. Visualization of ribosome-recycling factor on the Escherichia coli 70S ribosome: Functional implications. Proc Natl Acad Sci 101: 8900-8905.
3. Al Refaii A, Alix JH. 2009. Ribosome biogenesis is temperature-dependent and delayed in Escherichia coli lacking the chaperones DnaK or DnaJ. Mol Microbiol 71: 748-762.
4. Ali IK, Lancaster L, Feinberg J, Joseph S, Noller HF. 2006. Deletion of a conserved, central ribosomal intersubunit RNA bridge. Mol Cell 23: 865-874.
5. Antoun A, Pavlov MY, Tenson T, Ehrenberg MM. 2004. Ribosome formation from subunits studied by stopped-flow and Rayleigh light scattering. Biol Proced Online 6: 35-54.
6. Arluison V, Buckle M, Grosjean H. 1999. Pseudouridine synthetase Pus1 of Saccharomyces cerevisiae: Kinetic characterisation, tRNA structural requirement and real-time analysis of its complex with tRNA. J Mol Biol 289: 491-502. (Pubitemid 29295119)
7. Baba T, Ara T, Hasegawa M, Takai Y, Okumura Y, Baba M, Datsenko KA, Tomita M, Wanner BL, Mori H. 2006. Construction of Escherichia coli K-12 in-frame, single-gene knockout mutants: The Keio collection. Mol Syst Biol 2: doi: 10.1038/msb4100050.
8. Basturea GN, Deutscher MP. 2007. Substrate specificity and properties of the Escherichia coli 16S rRNA methyltransferase, RsmE. RNA 13: 1969-1976.
9. Blaha G, Burkhardt N, Nierhaus KH. 2002. Formation of 70S ribosomes: Large activation energy is required for the adaptation of exclusively the small ribosomal subunit. Biophys Chem 96: 153-161.
10. Blattner FR, Plunkett G, Bloch CA, Perna NT, Burland V, Riley M, Collado-Vides J, Glasner JD, Rode CK, Mayhew GF, et al. 1997. The complete genome sequence of Escherichia coli K-12. Science 5: 1453-1474.
11. Bradford MM. 1976. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72: 248-254.
12. Bremer H, Dennis PP. 1996. Modulation of chemical composition and other parameters of the cell growth rate. In Escherichia coli and Salmonella: Cellular and Molecular Biology, 2nd ed. (ed. FC Neidhardt et al.), pp. 1553-1568. American Society for Microbiology, Washington, DC.
13. Bügl H, Fauman EB, Staker BL, Zheng F, Kushner SR, Saper MA, Bardwell JC, Jakob U. 2000. RNA methylation under heat shock control. Mol Cell 6: 349-360.
14. Caldas T, Binet E, Bouloc P, Costa A, Desgres J, Richarme G. 2000a. The FtsJ/RrmJ heat shock protein of Escherichia coli is a 23 S ribosomal RNA methyltransferase. J Biol Chem 275: 16414-16419.
15. Caldas T, Binet E, Bouloc P, Richarme G. 2000b. Translational defects of Escherichia coli mutants deficient in the Um(2552) 23S ribosomal RNA methyltransferase RrmJ/FTSJ. Biochem Biophys Res Commun 271: 714-718.
16. Douthwaite S, Kirpekar F. 2007. Identifying modifications in RNA by MALDI mass spectrometry. Methods Enzymol 425: 1-20.
17. Ejby M, Sorensen MA, Pedersen S. 2007. Pseudouridylation of helix 69 of 23S rRNA is necessary for an effective translation termination. Proc Natl Acad Sci 104: 19410-19415.
18. Ero R, Peil L, Liiv A, Remme J. 2008. Identification of pseudouridine methyltransferase in Escherichia coli. RNA 14:2223-2233.
19. Gabashvili IS, Agrawal RK, Spahn CM, Grassucci RA, Svergun DI, Frank J, Penczek P. 2000. Solution structure of the E. coli 70S ribosome at 11.5 A resolution. Cell 100: 537-549.
20. Gegenheimer P, Watson N, Apirion D. 1977. Multiple pathways for primary processing of ribosomal RNA in Escherichia coli. J Biol Chem 252: 3064-3073.
21. Gehrke CW, Kuo KC. 1989. Ribonucleoside analysis by reversed-phase high-performance liquid chromatography. J Chromatogr 471: 3-36.
22. Gutgsell NS, Deutscher MP, Ofengand J. 2005. The pseudouridine synthase RluD is required for normal ribosome assembly and function in Escherichia coli. RNA 11: 1141-1152.
23. Hager J, Staker BL, Jakob U. 2004. Substrate binding analysis of the 23S rRNA methyltransferase RrmJ. J Bacteriol 186: 6634-6642. (Pubitemid 39258146)
24. Hamilton CS, Spedaliere CJ, Ginter JM, Johnston MV, Mueller EG. 2005. The roles of the essential Asp-48 and highly conserved His-43 elucidated by the pH dependence of the pseudouridine synthase TruB. Arch Biochem Biophys 433: 322-334.
25. Hennelly SP, Antoun A, Ehrenberg M, Gualerzi CO, Knight W, Lodmell JS, Hill WE. 2005. A time-resolved investigation of ribosomal subunit association. J Mol Biol 346: 1243-1258.
26. Hirabayashi N, Sato NS, Suzuki T. 2006. 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: 17203-17211.
27. Holmes KL, Culver GM. 2004. Mapping structural differences between 30S ribosomal subunit assembly intermediates. Nat Struct Mol Biol 11: 179-186.
28. Huang L, Ku J, Pookanjanatavip M, Gu X, Wang D, Greene PJ, Santi DV. 1998. Identification of two Escherichia coli pseudouridine synthases that show multisite specificity for 23S RNA. Biochemistry 37: 15951-15957.
29. Kaczanowska M, Rydén-Aulin M. 2007. Ribosome biogenesis and the translation process in Escherichia coli. Microbiol Mol Biol Rev 71: 477-494.
30. Kipper K, Hetenyi C, Sild S, Remme J, Liiv A. 2009. Ribosomal intersubunit bridge B2a is involved in factor-dependent translation initiation and translational processivity. J Mol Biol 385: 405-422.
31. Kowalak JA, Bruenger E, Hashizume T, Peltier JM, Ofengand J, McCloskey JA. 1996. Structural characterization of U*-1915 in domain IV from Escherichia coli 23S ribosomal RNA as 3-methylpseudouridine. Nucleic Acids Res 24: 688-693.
32. Leppik M, Peil L, Kipper K, Liiv A, Remme J. 2007. Substrate specificity of the pseudouridine synthase RluD in Escherichia coli. FEBS J 274: 5759-5766.
33. Lewicki BT, Margus T, Remme J, Nierhaus KH. 1993. Coupling of rRNA transcription and ribosomal assembly in vivo. Formation of active ribosomal subunits in Escherichia coli requires transcription of rRNA genes by host RNA polymerase which cannot be replaced by bacteriophage T7 RNA polymerase. J Mol Biol 231: 581-593.
34. Lindahl L. 1975. Intermediates and time kinetics of the in vivo assembly of Escherichia coli ribosomes. J Mol Biol 92: 15-37.
35. McClure WR. 1969. A kinetic analysis of coupled enzyme assays. Biochemistry 8: 2782-2786.
36. Mitchell P, Osswald M, Brimacombe R. 1992. Identification of intermolecular RNA cross-links at the subunit interface of the Escherichia coli ribosome. Biochemistry 31: 3004-3011.
37. Nierhaus KH. 1991. The assembly of prokaryotic ribosomes. Biochimie 73: 739-755.
38. O'Connor M, Dahlberg AE. 1995. The involvement of two distinct regions of 23 S ribosomal RNA in tRNA selection. J Mol Biol 254: 838-847.
39. Ofengand J. 2002. Ribosomal RNA pseudouridines and pseudouridine synthases. FEBS Lett 514: 17-25.
40. Ofengand J, Del Campo M. 2004. Modified nucleosides in Escherichia coli ribosomal RNA. In EcoSal - Escherichia coli and Salmonella: Cellular and Molecular Biology (ed. R. Curtiss), Chap. 4.6.1. ASM Press, Washington, DC.
41. Ofengand J, Malhotra A, Remme J, Gutgsell NS, Del Campo M, Jean-Charles S, Peil L, Kaya Y. 2001. Pseudouridines and pseudouridine synthases of the ribosome. Cold Spring Harb Symp Quant Biol 66: 147-159.
42. Okamoto S, Tamaru A, Nakajima C, Nishimura K, Tanaka Y, Tokuyama S, Suzuki Y, Ochi K. 2007. Loss of a conserved 7-methylguanosine modification in 16S rRNA confers low-level streptomycin resistance in bacteria. Mol Microbiol 63: 1096-1106.
43. Peil L, Virumae K, Remme J. 2008. Ribosome assembly in Escherichia coli strains lacking the RNA helicase DeaD/CsdA or DbpA. FEBS J 275: 3772-3782.
44. Purta E, Kaminska KH, Kasprzak JM, Bujnicki JM, Douthwaite S. 2008. YbeA is the m3Psi methyltransferase RlmH that targets nucleotide 1915 in 23S rRNA. RNA 14: 2234-2244.
45. Ramamurthy V, Swann SL, Spedaliere CJ, Mueller EG. 1999. Role of cysteine residues in pseudouridine synthases of different families. Biochemistry 38: 13106-13111.
46. Raychaudhuri S, Conrad J, Hall BG, Ofengand J. 1998. A pseudouridine synthase required for the formation of two universally conserved pseudouridines in ribosomal RNA is essential for normal growth of Escherichia coli. RNA 4: 1407-1417.
47. Sambrook J, Fritsch EF, Maniatis T. 1989. Molecular cloning: A laboratory manual, 2nd ed. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
48. Schuwirth BS, Borovinskaya MA, Hau CW, Zhang W, Vila-Sanjurjo A, Holton JM, Cate JH. 2005. Structures of the bacterial ribosome at 3.5 Å resolution. Science 310: 827-834.
49. Siibak T, Remme J. 2010. Subribosomal particle analysis reveals the stages of bacterial ribosome assembly at which rRNA nucleotides are modified. RNA doi: 10.1261/rna.2160010.
50. Srivastava AK, Schlessinger D. 1989. Processing pathway of Escherichia coli 16S precursor rRNA. Nucleic Acids Res 17: 1649-1663.
51. Storer AC, Cornish-Bowden A. 1974. The kinetics of coupled enzyme reactions. Applications to the assay of glucokinase, with glucose 6-phosphate dehydrogenase as coupling enzyme. Biochem J 141: 205-209.
52. Vaidyanathan PP, Deutscher MP, Malhotra A. 2007. RluD, a highly conserved pseudouridine synthase, modifies 50S subunits more specifically and efficiently than free 23S rRNA. RNA 13: 1868-1876.
53. Yusupov MM, Yusupova GZ, Baucom A, Lieberman K, Earnest TN, Cate JH, Noller HF. 2001. Crystal structure of the ribosome at 5.5 Å resolution. Science 292: 883-896.