RluD, a highly conserved pseudouridine synthase, modifies 50S subunits more specifically and efficiently than free 23S rRNA

RNA

Volumn 13, Issue 11, 2007, Pages 1868-1876

  Vaidyanathan, Pavanapuresan P ^a   Deutscher, Murray P ^a   Malhotra, Arun ^a  

^a UNIVERSITY OF MIAMI MILLER SCHOOL OF MEDICINE   (United States)

Author keywords

Pseudouridine; Ribosome biogenesis; RluD; RNA modification

Indexed keywords

ESCHERICHIA COLI PROTEIN; PROTEIN RLUD; PSEUDOURIDINE; RIBOSOME RNA; UNCLASSIFIED DRUG;

ARTICLE; ESCHERICHIA COLI; PRIORITY JOURNAL; PROTEIN MODIFICATION; RIBOSOME SUBUNIT; RNA STRUCTURE; SEQUENCE ANALYSIS;

ESCHERICHIA COLI PROTEINS; HYDRO-LYASES; MODELS, MOLECULAR; PROTEIN STRUCTURE, TERTIARY; RIBOSOME SUBUNITS, LARGE, BACTERIAL; RNA, RIBOSOMAL, 23S; SUBSTRATE SPECIFICITY;

ESCHERICHIA COLI;

EID: 35548946655     PISSN: 13558382     EISSN: 14699001     Source Type: Journal    
DOI: 10.1261/rna.711207     Document Type: Article

References (54)

1. Ali, I.K., Lancaster, L., Feinberg, J., Joseph, S., and Noller, H.F. 2006. Deletion of a conserved, central ribosomal intersubunit RNA bridge. Mol. Cell 23: 865-874.
2. Andersen, N.M. and Douthwaite, S. 2006. YebU is a m5C methyltransferase specific for 16 S rRNA nucleotide 1407. J. Mol. Biol. 359: 777-786.
3. Bashan, A., Agmon, I., Zarivach, R., Schluenzen, F., Harms, J., Berisio, R., Bartels, H., Franceschi, F., Auerbach, T., Hansen, H.A., et al. 2003. Structural basis of the ribosomal machinery for peptide bond formation, translocation, and nascent chain progression. Mol. Cell 11: 91-102.
4. Basturea, G.N. and Deutscher, M.P. 2007. Substrate specificity and properties of the Escherichia coli 16S rRNA methyltransferase, RsmE. RNA (this issue) doi: 10.1261/rna.700507.
5. Baxter-Roshek, J.L., Petrov, A.N., and Dinman, J.D. 2007. Optimization of ribosome structure and function by rRNA base modification. PLoS ONE 2: e174. doi: 10.1371/journal.pone.0000174.
6. Bügl, H., Fauman, E.B., Staker, B.L., Zheng, F., Kushner, S.R., Saper, M.A., Bardwell, J.C., and Jakob, U. 2000. RNA methylation under heat shock control. Mol. Cell 6: 349-360.
7. Phe. Nucleic Acids Res. 33: 6961-6971. doi: 10.1093/nar/gki1004.
8. Charette, M. and Gray, M.W. 2000. Pseudouridine in RNA: What, where, how, and why. IUBMB Life 49: 341-351.
9. Culver, G.M. 2003. Assembly of the 30S ribosomal subunit. Biopolymers 68: 234-249.
10. Datsenko, K.A. and Wanner, B.L. 2000. One-step inactivation of chromosomal genes in Escherichia coli K-12 using PCR products, Proc. Natl. Acad. Sci. 97: 6640-6645.
11. 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.
12. Davis, I.W., Murray, L.W., Richardson, J.S., and Richardson, D.C. 2004. MolProbity: Structure validation and all-atom contact analysis for nucleic acids and their complexes. Nucleic Acids Res. 32: W615-W619. doi: 10.1093/nar/gkh398.
13. 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.
14. Del Campo, M., Ofengand, J., and Malhotra, A. 2003. Purification and crystallization of Escherichia coli pseudouridine synthase RluD. Acta Crystallogr. D Biol. Crystallogr. 59: 1871-1873.
15. Del Campo, M., Ofengand, J., and Malhotra, A. 2004. Crystal structure of the catalytic domain of RluD, the only rRNA pseudouridine synthase required for normal growth of Escherichia coli. RNA 10: 231-239.
16. DeLano, W.L. 2002. The PyMOL user's manual. DeLano Scientific, Palo Alto, CA.
17. Deutscher, M.P., Marlor, C.W., and Zaniewski, R. 1984. Ribonuclease T: New exoribonuclease possibly involved in end-turnover of tRNA. Proc. Natl. Acad. Sci. 81: 4290-4293.
18. Dlakić, M. 2005. The ribosomal subunit assembly line. Genome Biol. 6: 234. doi: 10.1186/gb-2005-6-10-234.
19. Emsley, P. and Cowtan, K. 2004. Coot: Model-building tools for molecular graphics. Acta Crystallogr. D: Biol. Crystallogr. 60: 2126-2132.
20. Gutgsell, N.S., Deutscher, M.P., and Ofengand, J. 2005. The pseudouridine synthase RluD is required for normal ribosome assembly and function in Escherichia coli. RNA 11: 1141-1152.
21. Hansen, L.H., Kirpekar, F., and Douthwaite, S. 2001. Recognition of nucleotide G745 in 23 S ribosomal RNA by the rrmA methyltransferase. J. Mol. Biol. 310: 1001-1010.
22. Hirabayashi, N., Sato, N.S., and 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.
23. 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.
24. Hoang, C., Chen, J., Vizthum, C.A., Kandel, J.M., Hamilton, C.S., Mueller, E.G., and Ferré-D'Amaré, A.R. 2006. Crystal structure of pseudouridine synthase RluA: Indirect sequence readout through protein-induced RNA structure. Mol. Cell 24: 535-545.
25. Huang, L., Ku, J., Pookanjanatavip, M., Gu, X., Wang, D., Greene, P.J., and Santi, D.V. 1998. Identification of two Escherichia coli pseudouridine synthases that show multisite specificity for 23S RNA. Biochemistry 37: 15951-15957.
26. Hur, S., Stroud, R.M., and Finer-Moore, J. 2006. Substrate recognition by RNA M5U methyltransferases and pseudouridine synthases: A structural perspective. J. Biol. Chem. 281: 38969-38973.
27. Jiang, M., Datta, K., Walker, A., Strahler, J., Bagamasbad, P., Andrews, P.C., and Maddock, J.R. 2006. The Escherichia coli GTPase CgtAE is involved in late steps of large ribosome assembly. J. Bacteriol. 188: 6757-6770.
28. King, T.H., Liu, B., McCully, R.R., and Fournier, M.J. 2003. Ribosome structure and activity are altered in cells lacking snoRNPs that form pseudouridines in the peptidyl transferase center. Mol. Cell 11: 425-435.
29. Klein, D.J., Moore, P.B., and Steitz, T.A. 2004. The roles of ribosomal proteins in the structure assembly, and evolution of the large ribosomal subunit. J. Mol. Biol. 340: 141-177.
30. Kleywegt, G.J., Zou, J.Y., Kjeldgaard, M., and Jones, T.A. 2001. Around O. In International tables for crystallography (eds. M.G. Rossmann and E. Arnold), Vol. F, pp. 353-356. Kluwer Academic Publishers, Dordrecht, The Netherlands.
31. Korostelev, A., Trakhanov, S., Laurberg, M., and Noller, H.F. 2006. Crystal structure of a 70S ribosome-tRNA complex reveals functional interactions and rearrangements. Cell 126: 1065-1077.
32. Krissinel, E. and Henrick, K. 2004. Secondary structure matching (SSM), a new tool for fast protein structure alignment in three dimensions. Acta Crystallogr. D: Biol. Crystallogr. 60: 2256-2268.
33. LaRiviere, F.J., Cole, S.E., Ferullo, D.J., and Moore, M.J. 2006. A late-acting quality control process for mature eukaryotic rRNAs. Mol. Cell 24: 619-626.
34. Liang, X.H., Xu, Y.X., and Michaeli, S. 2002. The spliced leader-associated RNA is a trypanosome-specific sn(o) RNA that has the potential to guide pseudouridine formation on the SL RNA. RNA 8: 237-246.
35. Liiv, A., Karitkina, D., Maiväli, U., and Remme, J. 2005. Analysis of the function of E. coli 23S rRNA helix-loop 69 by mutagenesis. BMC Mol. Biol. 6: 18. doi: 10.1186/1471-2199-6-18.
36. 5U1939 in 23S rRNA using MALDI mass spectrometry. Nucleic Acids Res. 31: 4738-4746. doi: 10.1093/nar/gkg657.
37. Mizutani, K., Machida, Y., Unzai, S., Park, S.Y., and Tame, J.R. 2004. Crystal structures of the catalytic domains of pseudouridine synthases RluC and RluD from Escherichia coli. Biochemistry 43: 4454-4463.
38. Nazar, R.N. 2004. Ribosomal RNA processing and ribosome biogenesis in eukaryotes. IUBMB Life 56: 457-465.
39. Ofengand, J., Malhotra, A., Remme, J., Gutgsell, N.S., Del Campo, M., Jean-Charles, S., Peil, L., and Kaya, Y. 2001. Pseudouridines and pseudouridine synthases of the ribosome. Cold Spring Harb. Symp. Quant. Biol. 66: 147-159.
40. Powers, T. and Noller, H.F. 1995. Hydroxyl radical footprinting of ribosomal proteins on 16S rRNA. RNA 1: 194-209.
41. Raychaudhuri, S., Conrad, J., Hall, B.G., and 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.
42. 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.
43. Rozenski, J., Crain, P.F., and McCloskey, J.A. 1999. The RNA Modification Database: 1999 update. Nucleic Acids Res. 27: 196-197. doi: 10.1093/nar/27.1.196.
44. Schuwirth, B.S., Borovinskaya, M.A., Hau, C.W., Zhang, W., Vila-Sanjurjo, A., Holton, J.M., and Cate, J.H. 2005. Structures of the bacterial ribosome at 3.5 Å resolution. Science 310: 827-834.
45. Selmer, M., Dunham, C.M., Murphy, F.V., Weixlbaumer, A., Petry, S., Kelley, A.C., Weir, J.R., and Ramakrishnan, V. 2006. Structure of the 70S ribosome complexed with mRNA and tRNA. Science 313: 1935-1942.
46. Sivaraman, J., Sauvé, V., Larocque, R., Stura, E.A., Schrag, J.D., Cygler, M., and Matte, A. 2002. Structure of the 16S rRNA pseudouridine synthase RsuA bound to uracil and UMP. Nat. Struct. Biol. 9: 353-358.
47. Sivaraman, J., Iannuzzi, P., Cygler, M., and Matte, A. 2004. Crystal structure of the RluD pseudouridine synthase catalytic module, an enzyme that modifies 23S rRNA and is essential for normal cell growth of Escherichia coli. J. Mol. Biol. 335: 87-101.
48. Song, X. and Nazar, R.N. 2002. Modification of rRNA as a "quality control mechanism" in ribosome biogenesis. FEBS Lett. 523: 182-186.
49. Talkington, M.W., Siuzdak, G., and Williamson, J.R. 2005. An assembly landscape for the 30S ribosomal subunit. Nature 438: 628-632.
50. Tscherne, J.S., Nurse, K., Popienick, P., and Ofengand, J. 1999. Purification, cloning, and characterization of the 16 S RNA m2G1207 methyltransferase from Escherichia coli. J. Biol. Chem. 274: 924-929.
51. Weitzmann, C.J., Cunningham, P.R., and Ofengand, J. 1990. Cloning, in vitro transcription, and biological activity of Escherichia coli 23S ribosomal RNA. Nucleic Acids Res. 18: 3515-3520. doi: 10.1093/nar/18.12.3515.
52. Wrzesinski, J., Bakin, A., Nurse, K., Lane, B.G., and Ofengand, J. 1995. Purification, cloning, and properties of the 16S RNA pseudouridine 516 synthase from Escherichia coli. Biochemistry 34: 8904-8913.
53. Wrzesinski, J., Bakin, A., Ofengand, J., and Lane, B.G. 2000. Isolation and properties of Escherichia coli 23S-RNA pseudouridine 1911, 1915, 1917 synthase (RluD). IUBMB Life 50: 33-37.
54. Yusupov, M.M., Yusupova, G.Z., Baucom, A., Lieberman, K., Earnest, T.N., Cate, J.H., and Noller, H.F. 2001. Crystal structure of the ribosome at 5.5 Å resolution. Science 292: 883-896.