Influence of phylogeny on posttranscriptional modification of rRNA in thermophilic prokaryotes: The complete modification map of 16S rRNA of Thermus thermophilus

Biochemistry

Volumn 45, Issue 15, 2006, Pages 4888-4899

  Guymon, Rebecca ^a   Pomerantz, Steven C ^a   Crain, Pamela F ^a   McCloskey, James A ^a,b  

^a UNIVERSITY OF UTAH   (United States)

^b UNIVERSITY OF UTAH SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIA; ESCHERICHIA COLI; IONIZATION; STABILIZATION; THERMODYNAMIC STABILITY;

POSTTRANSCRIPTIONAL MODIFICATION; SULFOLOBUS SOLFATARICUS; THERMUS MODIFICATION;

RNA;

PSEUDOURIDINE; RIBONUCLEASE; RIBOSOME RNA; RNA 16S; SMALL SUBUNIT RIBOSOMAL RNA;

ARTICLE; BACTERIAL GROWTH; COMPUTER PROGRAM; ELECTROSPRAY MASS SPECTROMETRY; ESCHERICHIA COLI; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; HYDROLYSIS; INCUBATION TEMPERATURE; METHYLATION; NONHUMAN; PHYLOGENY; PRIORITY JOURNAL; PROKARYOTE; RNA PROCESSING; RNA STRUCTURE; STOICHIOMETRY; SULFOLOBUS SOLFATARICUS; TANDEM MASS SPECTROMETRY; THERMOSTABILITY; THERMUS THERMOPHILUS;

BASE SEQUENCE; CHROMATOGRAPHY, LIQUID; MODELS, BIOLOGICAL; MOLECULAR SEQUENCE DATA; PHYLOGENY; PROKARYOTIC CELLS; RIBONUCLEASES; RNA PROCESSING, POST-TRANSCRIPTIONAL; RNA, RIBOSOMAL, 16S; SPECTROMETRY, MASS, ELECTROSPRAY IONIZATION; THERMUS THERMOPHILUS;

ARCHAEA; BACTERIA (MICROORGANISMS); ESCHERICHIA COLI; PROKARYOTA; SULFOLOBUS; SULFOLOBUS SOLFATARICUS; THERMUS; THERMUS THERMOPHILUS;

EID: 33645943707     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi052579p     Document Type: Article

References (63)

1. Grosjean, H., and Benne, R., Eds. (1998) Modification and Editing of RNA, pp 596, ASM Press, Washington, DC.
2. Agris, P. F. (2004) Decoding the genome: a modified view, Nucleic Acids Res. 32, 223-238.
3. Rozenski, J., Crain, P. F., and McCloskey, J. A. (1999) The RNA modification database-1999 update, Nucleic Acids Res. 27, 196-197.
4. Sprinzl, M., and Vassilenko, K. S. (2005) Compilation of tRNA sequences and sequences of tRNA genes, Nucleic Acids Res. 33, D139-D140.
5. Maden, B. E. H. (1990) The numerous modified nucleosides in eukaryotic ribosomal RNA, Prog. Nucleic Acid Res. Mol. Biol. 39, 241-303.
6. Bakin, A., Kowalak, J. A., McCloskey, J. A., and Ofengand, J. (1994) A single pseudouridine residue in E. coli 16S RNA is located at position 516, Nucleic Acids Res. 22, 3681-3684.
7. Gupta, R., Lanter, J. M., and Woese, C. R. (1983) Sequence of the 16S ribosomal RNA from Halobacterium volcanii, an archae-bacterium, Science 221, 656-659.
8. Kowalak, J., Bruenger, E., Crain, P. F., and McCloskey, J. A. (2000) Identities and phylogenetic comparisons of posttranscriptional modifications in 16S ribosomal RNA from Haloferax volcanii, J. Biol. Chem. 275, 24484-24489.
9. Rozenski, J., and McCloskey, J. A. (2005) The small subunit rRNA modification database, Nucleic Acids Res. 33, D135-D138.
10. Balch, W. E., Fox, G. E., Magrum, L. J., Woese, C. R., and Wolfe, R. S. (1979) Methanogens: reevaluation of a unique biological group, Microbiol. Rev. 43, 260-296.
11. Fox, G. E., Pechman, K. R., and Noese, C. R. (1977) Comparative cataloging of 16S ribosomal RNA: molecular approach to procaryotic systematics, Int. J. Syst. Bacteriol. 27, 44-57.
12. Ofengand, J., and Fournier, M. J. (1998) The pseudouridine residues of rRNA: number, location, biosynthesis, and function, in Modification and Editing of RNA (Grosjean, H., and Benne, R., Eds.) pp 229-253, ASM Press, Washington, DC.
13. Charette, M., and Gray, M. W. (2000) Pseudouridine in RNA: what, where, how, and why, IUBMB Life 49, 341-351.
14. Noon, K. R., Bruenger, E., and McCloskey, J. A. (1998) Posttranscriptional modifications in 16S and 23S rRNAs of the archaeal hyperthermophile Sulfolobus solfataricus, J. Bacteriol. 180, 2883-2888.
15. Oshima, T., and Imahori (1974) Description of Thermus thermophilus (Yoshida and Oshima) comb, nob., a nonsporulating thermophilic bacterium from a Japanese thermal spa, Int. J. Syst. Bacteriol. 24, 102-112.
16. Kowalak, J. A., Bruenger, E., and McCloskey, J. A. (1995) Posttranscriptional modification of the central loop of domain V in E. coli 23S ribosomal RNA, J. Biol. Chem. 270, 17758-17764.
17. Crain, P. F., Ruffner, D. E., Ho, Y., Qiu, F., Rozenski, J., and McCloskey, J. A. (1999) Problems and prospects in the characterization of posttranscriptional modifications in large RNAs, in Mass Spectrometry in Biology and Medicine (Burlingame, A. L., Carr, S. A., and Baldwin, M. A., Eds.) pp 531-551, Humana Press, Totowa, NJ.
18. Kowalak, J. A., Bruenger, E., Crain, P. F., and McCloskey, J. A. (2000) Identities and phylogenetic comparisons of posttranscriptional modifications in 16S ribosomal RNA from Haloferax volcanii, J. Biol. Chem. 275, 24484-24489.
19. Hansen, L. H., Kirpekar, F., and Douthwaite, S. (2001) Recognition of nucleotide G745 in 23S ribosomal RNA by the rrmA methyl-transferase, J. Mol. Biol. 310, 1001-1010.
20. Hansen, M. A., Kirpekar, F., Ritterbusch, W., and Vester, B. (2002) Posttranscriptional modifications in the A-loop of 23S rRNAs from selected archaea and eubacteria, RNA 8, 202-213.
21. Andersen, T. E., Porse, B. T., and Kirpekar, F. (2004) A novel partial modification at C2501 in Escherichia coli 23S ribosomal RNA, RNA 10, 907-913.
22. Kirpekar, F., Hansen, L. H., Rasmussen, A., Poehlsgaard, J., and Vester, B. (2005) The archaeon Haloarcula marismortui has few modifications in the central parts of its 23S ribosomal RNA, J. Mol. Biol. 348, 563-573.
23. Chomczynski, P., and Sacchi, N. (1987) Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction, Anal. Biochem. 162, 156-159.
24. Crain, P. F. (1990) Preparation and enzymatic hydrolysis of RNA and DNA for mass spectrometry, Methods Enzymol. 193, 782-790.
25. Pomerantz, S. C., and McCloskey, J. A. (1990) Analysis of RNA hydrolyzates by LC/MS, Methods Enzymol. 193, 796-824.
26. opt 95 °C), J. Bacteriol. 185, 5483-5490.
27. Apffel, A., Chakel, J. A., Fischer, S., Lichtenwalter, K., and Hancock, W. S. (1997) Analysis of oligonucleotides by HPLC-electrospray ionization mass spectrometry, Anal. Chem. 69, 1320-1325.
28. Ni, J., Pomerantz, S. C., Rozenski, J., Zhang, Y., and McCloskey, J. A. (1996) Interpretation of oligonucleotide mass spectra for determination of sequence using electrospray ionization and tandem mass spectrometry, Anal. Chem. 68, 1989-1999.
29. Rozenski, J., and McCloskey, J. A. (2002) SOS: a simple interactive program for ab initio oligonucleotide sequencing by mass spectrometry, J. Am. Soc. Mass Spectrom. 13, 200-203.
30. 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.
31. McLuckey, S. A., Van Berkel, G. J., and Glish, G. L. (1992) Tandem mass spectrometry of small, multiply charged oligonucleotides, J. Am. Soc. Mass Spectrom. 3, 60-70.
32. 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.
33. Pomerantz, S. C., Kowalak, J. A., and McCloskey, J. A. (1993) Determination of oligonucleotide composition from mass spectrometrically measured molecular weight, J. Am. Soc. Mass Spectrom. 4, 204-209.
34. Kowalak, J. A., Pomerantz, S. C., Crain, P. F., and McCloskey, J. A. (1993) A novel method for the determination of posttransciptional modification in RNA by mass spectrometry, Nucleic Acids Res. 21, 4577-4585.
35. Limbach, P. A., Crain, P. F., and McCloskey, J. A. (1994) Summary: the modified nucleosides of RNA, Nucleic Acids Res. 22, 2183-2196.
36. van Knippenberg, P. H., Van Kimmenade, J. M., and Heus, H. A. (1984) Phylogeny of the conserved 3′ terminal structure of the RNA of small ribosomal subunits, Nucleic Acids Res. 12, 2595-2604.
37. 6-dimethyladenosine in 16S ribosomal RNA, in Structure, Function, and Genetics of Ribosomes (Hardesty, B., and Kramer, G., Eds.) pp 412-424, Springer-Verlag, New York.
38. Woese, C. R. (1987) Bacterial evolution, Microbiol. Rev. 51, 221-271.
39. Wimberly, B. T., Brodersen, D. E., Clemons, W. M., Jr., Morgan-Warren, R. J., Carter, A. P., Vonrhein, C., Hartsch, T., and Ramakrishnan, V. (2000) Structure of the 30S ribosomal subunit, Nature 407, 327-339.
40. 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.
41. Pace, N. R. (1997) A molecular view of microbial diversity and the biosphere, Science 276, 734-740.
42. Woese, C. R., Gutell, R., Gupta, R., and Noller, H. F. (1983) Detailed analysis of the higher-order structure of 16S-like ribonucleic acids, Microbiol. Rev. 47, 621-669.
43. Sampson, J. R., and Uhlenbeck, O. C. (1988) Biochemical and physical characterization of an unmodified yeast phenylalanine transfer RNA transcribed in vitro, Proc. Natl. Acad. Sci. U.S.A. 85, 1033-1037.
44. Derrick, W. B., and Horowitz, J. (1993) Probing structural differences between native and in vitro transcribed Escherichia coli valine transfer RNA: evidence for stable base modification-dependent conformers, Nucleic Acids Res. 21, 4948-4953.
45. Kowalak, J. A., Dalluge, J. J., McCloskey, J. A., and Stetter, K. O. (1994) Role of posttranscriptional modification in stabilization of transfer RNA from hyperthermophiles, Biochemistry 33, 7869-7876.
46. Kawai, G., Ue, H., Yasuda, M., Sakamoto, K., Hashizume, T., McCloskey, J. A., Miyazawa, T., and Yokoyama, S. (1991) Relation between functions and conformational characteristics of modified nucleosides found in tRNAs, Nucleic Acids Symp. Ser., 49-50.
47. Kawai, G., Yamamoto, Y., Kamimura, T., Masegi, T., Sekine, M., Hata, T., Iimori, T., Watanabe, T., Miyazawa, T., and Yokoyama, S. (1992) Conformational rigidity of specific pyrimidine residues in tRNA arises from posttranscriptional modifications that enhance steric interaction between the base and the 2′hydroxyl group, Biochemistry 31, 1040-1046.
48. Davis, D. R. (1998) Biophysical and conformational properties of modified nucleosides in RNA (nuclear magnetic resonance studies), in Modification and Editing of RNA (Grosjean, H., and Benne, R., Eds.) pp 85-102, ASM Press, Washington, DC.
49. Carbon, P., Ebel, J. P., and Ehresmann, C. (1981) The sequence of the ribosomal 16S RNA from Proteus vulgaris. Sequence comparison with E. coli 16S RNA and its use in secondary structure modeling, Nucleic Acids Res. 9, 2325-2333.
50. Hensel, R., Demharter, W., Kandler, O., Kroppenstedt, R. M., and Stackebrandt, E. (1986) Chemotaxonomic and molecular-genetic studies of the genus Thermus. Evidence for a phylogenetic relationship of Thermus aquaticus and Thermus ruber to the genus Deinococcus, Int. J. Syst. Bacteriol. 36, 444-453.
51. Brimacombe, R., Mitchell, P., Osswald, M., Stade, K., and Bochkariov, D. (1993) Clustering of modified nucleotides at the functional center of the ribosome, FASEB J. 7, 161-167.
52. 2+ and a conformational transition at the anticodon stem-loop of yeast phenylalanine tRNA, Biochemistry 32, 10249-10253.
53. Sowers, L. C., Shaw, B. R., and Sedwick, W. D. (1987) Base stacking and molecular polarizability: effect of a methyl group in the 5-position of pyrimidines, Biochem. Biophys. Res. Commun. 148, 790-794.
54. Wang, S., and Kool, E. T. (1995) Origins of the large differences in stability of DNA and RNA helices: C-5 methyl and 2′-hydroxyl effects, Biochemistry 34, 4125-4132.
55. Ofengand, J. (2002) Ribosomal RNA pseudouridines and pseudouridine synthases, FEBS Lett. 514, 17-25.
56. Del Campo, M., Recinos, C., Yanez, G., Pomerantz, S. C., Guymon, R., Crain, P. F., McCloskey, J. A., and Ofengand, J. (2005) Number, position, and significance of the pseudouridines in the large subunit ribosomal RNA of Haloarcula marismortui and Deinococcus radiodurans, RNA II, 210-219.
57. Woese, C. R., Gupta, R., Hahn, C. M., Zillig, W., and Tu, J. (1984) The phylogenetic relationships of three sulfur dependent archaebacteria, Syst. Appl. Microbiol. 5, 97-105.
58. 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.
59. Meroueh, M., Grohar, P. J., Qiu, J., SantaLucia, J., J., Scaringe, S. A., and Chow, C. S. (2000) Unique structural and stabilizing roles for the individual pseudouridine residues in the 1920 region of Escherichia coli 23S rRNA, Nucleic Acids Res. 28, 2075-2083.
60. Davis, D. R. (1995) Stabilization of RNA stacking by pseudo-uridine, Nucleic Acids Res. 23, 5020-5026.
61. 15N NMR studies of Escherichia coli tRNA(Phe) from hisT mutants: a structural role for pseudouridine, Biochemistry 30, 4223-4231.
62. Tyr, J. Biomol. Struct. Dyn. 15, 1121-1132.
63. Qiu, F., and McCloskey, J. A. (1999) Selective detection of ribose-methylated nucleotides in RNA by a mass spectrometry based method, Nucleic Acids Res. 27, e20.