Structural and functional studies of the Thermus thermophilus 16S rRNA methyltransferase RsmG

RNA

Volumn 15, Issue 9, 2009, Pages 1693-1704

  Gregory, Steven T ^a   Demirci, Hasan ^a   Belardinelli, Riccardo ^a,b   Monshupanee, Tanakarn ^a   Gualerzi, Claudio ^b   Dahlberg, Albert E ^a   Jogl, Gerwald ^a  

^a BROWN UNIVERSITY   (United States)

^b UNIVERSITY OF CAMERINO   (Italy)

Author keywords

16S rRNA; 7 Methylguanine; Methyltransferase; Ribosome modification; S adenosyl L methionine

Indexed keywords

ADENOSINE PHOSPHATE; MAGNESIUM; RNA 16S; RNA 30S; RNA DERIVATIVE; RNA METHYLTRANSFERASE; STREPTOMYCIN; UNCLASSIFIED DRUG;

ANTIBIOTIC RESISTANCE; ARTICLE; BACTERIAL GENE; BACTERIAL STRAIN; BACTERIUM MUTANT; CONCENTRATION (PARAMETERS); CRYSTAL STRUCTURE; ENZYME ACTIVE SITE; ENZYME SUBSTRATE; GENE ACTIVITY; GENE DELETION; GENE IDENTIFICATION; GENE ISOLATION; GENETIC CONSERVATION; NONHUMAN; NUCLEOTIDE SEQUENCE; PHENOTYPE; PRIORITY JOURNAL; RIBOSOME SUBUNIT; RNA METHYLATION; RSMG GENE; THERMUS THERMOPHILUS;

AMINO ACID SEQUENCE; BASE SEQUENCE; CATALYTIC DOMAIN; CRYSTALLOGRAPHY, X-RAY; DRUG RESISTANCE, BACTERIAL; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; MUTANT PROTEINS; NUCLEIC ACID CONFORMATION; ORGANISMS, GENETICALLY MODIFIED; PHENOTYPE; RIBOSOME SUBUNITS, SMALL, BACTERIAL; RNA, RIBOSOMAL, 16S; SEQUENCE HOMOLOGY, AMINO ACID; STREPTOMYCIN; THERMUS THERMOPHILUS; TRNA METHYLTRANSFERASES;

ESCHERICHIA COLI; THERMUS THERMOPHILUS;

EID: 69049112874     PISSN: 13558382     EISSN: 14699001     Source Type: Journal    
DOI: 10.1261/rna.1652709     Document Type: Article

References (55)

1. Adams PD, Grosse-Kunstleve RW, Hung LW, Ioerger TR, McCoy AJ, Moriarty NW, Read RJ, Sacchettini JC, Sauter NK, Terwilliger TC. 2002. PHENIX: Building new software for automated crystallographic structure determination. Acta Crystallogr D Biol Crystallogr 58: 1948-1954.
2. Bailey S. 1994. The CCP4 Suite - programs for protein crystallography. Acta Crystallogr D Biol Crystallogr 50: 760-763.
3. Baker NA, Sept D, Joseph S, Holst MJ, McCammon JA. 2001. Electrostatics of nanosystems: Application to microtubules and the ribosome. Proc Natl Acad Sci 98: 10037-10041.
4. Beeby M, O'Connor BD, Ryttersgaard C, Boutz DR, Perry LJ, Yeates TO. 2005. The genomics of disulfide bonding and protein stabilization in thermophiles. PLoS Biol 3: e309. doi: 10.1371/journal.pbio. 0030309.
5. Carr JF, Gregory ST, Dahlberg AE. 2005. Severity of the streptomycin resistance and streptomycin dependence phenotypes of ribosomal protein S12 of Thermus thermophilus depends on the identity of highly conserved amino acid residues. J Bacteriol 187: 3548-3550.
6. Carter AP, Clemons WM, Brodersen DE, Morgan-Warren RJ, Wimberly BT, Ramakrishnan V. 2000. Functional insights from the structure of the 30S ribosomal subunit and its interactions with antibiotics. Nature 407: 340-348.
7. Chow CS, Lamichhane TN, Mahto SK. 2007. Expanding the nucleotide repertoire of the ribosome with post-transcriptional modifications. ACS Chem Biol 2: 610-619.
8. Clamp M, Cuff J, Searle SM, Barton GJ. 2004. The Jalview Java alignment editor. Bioinformatics 20: 426-427.
9. Cohen SX, Morris RJ, Fernandez FJ, Ben Jelloul M, Kakaris M, Parthasarathy V, Lamzin VS, Kleywegt GJ, Perrakis A. 2004. Toward complete validated models in the next generation of ARP/wARP. Acta Crystallogr D Biol Crystallogr 60: 2222-2229.
10. Davis IW, Leaver-Fay A, Chen VB, Block JN, Kapral GJ, Wang X, Murray LW, Arendall WB, Snoeyink J, Richardson JS, et al. 2007. MolProbity: All-atom contacts and structure validation for proteins and nucleic acids. Nucleic Acids Res 35: W375-W383.
11. Decatur WA, Fournier MJ. 2002. rRNA modifications and ribosome function. Trends Biochem Sci 27: 344-351.
12. Demirci H, Gregory ST, Dahlberg AE, Jogl G. 2007. Recognition of ribosomal protein L11 by the protein trimethyltransferase PrmA. EMBO J 26: 567-577.
13. Demirci H, Gregory ST, Dahlberg AE, Jogl G. 2008a. Crystal structure of the Thermus thermophilus 16 S rRNA methyltransferase RsmC in complex with cofactor and substrate guanosine. J Biol Chem 283: 26548-26556.
14. Demirci H, Gregory ST, Dahlberg AE, Jogl G. 2008b. Multiple-site trimethylation of ribosomal protein L11 by the PrmA methyltransferase. Structure 16: 1059-1066.
15. Demirci H, Belardinelli R, Seri E, Gregory ST, Gualerzi C, Dahlberg AE, Jogl G. 2009. Structural rearrangements in the active site of the Thermus thermophilus 16S rRNA methyltransferase KsgA in a binary complex with 5′-methylthioadenosine. J Mol Biol 388: 271-282.
16. Emsley P, Cowtan K. 2004. Coot: Model-building tools for molecular graphics. Acta Crystallogr D Biol Crystallogr 60: 2126-2132.
17. Fabrega C, Hausmann S, Shen V, Shuman S, Lima CD. 2004. Structure and mechanism of mRNA cap (guanine-N7) methyltransferase. Mol Cell 13: 77-89.
18. Fiser A, Sali A. 2003. Modeller: Generation and refinement of homology-based protein structure models. Methods Enzymol 374: 461-491.
19. Gregory ST, Dahlberg AE. 2008. Transposition of an insertion sequence, ISTth7, in the genome of the extreme thermophile Thermus thermophilus HB8. FEMS Microbiol Lett 289: 187-192.
20. Gregory ST, Dahlberg AE. 2009. Genetic and structural analysis of base substitutions in the central pseudoknot of Thermus thermophilus 16S ribosomal RNA. RNA 15: 215-223.
21. Gregory ST, Cate JHD, Dahlberg AE. 2001. Streptomycin-resistant and streptomycin-dependent mutants of the extreme thermophile Thermus thermophilus. J Mol Biol 309: 333-338.
22. Gregory ST, Carr JF, Dahlberg AE. 2009. A signal relay between ribosomal protein S12 and elongation factor EF-Tu during decoding of mRNA. RNA 15: 208-214.
23. Gustilo EM, Vendeix FA, Agris PF. 2008. tRNA's modifications bring order to gene expression. Curr Opin Microbiol 11: 134-140.
24. Guymon R, Pomerantz SC, Crain PF, McCloskey JA. 2006. Influence of phylogeny on post-transcriptional modification of rRNA in thermophilic prokaryotes: The complete modification map of 16S rRNA of Thermus thermophilus. Biochemistry 45: 4888-4899.
25. Hashimoto Y, Yano T, Kuramitsu S, Kagamiyama H. 2001. Disruption of Thermus thermophilus genes by homologous recombination using a thermostable kanamycin-resistant marker. FEBS Lett 506: 231-234.
26. Helser TL, Davies JE, Dahlberg JE. 1972. Mechanism of kasugamycin resistance in Escherichia coli. Nat New Biol 235: 6-9.
27. Holm L, Kaariainen S, Rosenstrom P, Schenkel A. 2008. Searching protein structure databases with DaliLite v.3. Bioinformatics 24: 2780-2781.
28. Ireton K, Gunther NW, Grossman AD. 1994. spo0J is required for normal chromosome segregation as well as the initiation of sporulation in Bacillus subtilis. J Bacteriol 176: 5320-5329.
29. Johansen SK, Maus CE, Plikaytis BB, Douthwaite S. 2006. Capreomycin binds across the ribosomal subunit interface using tlyA-encoded 2′-O- methylations in 16S and 23S rRNAs. Mol Cell 23: 173-182.
30. Kinghorn SM, O'Byrne CP, Booth IR, Stansfield I. 2002. Physiological analysis of the role of truB in Escherichia coli: A role for tRNA modification in extreme temperature resistance. Microbiology 148: 3511-3520.
31. Koyama Y, Hoshino T, Tomizuka N, Furukawa K. 1986. Genetic transformation of the extreme thermophile Thermus thermophilus and of other Thermus spp. J Bacteriol 166: 338-340.
32. Krol A, Carbon P. 1989. A guide for probing native small nuclear RNA and ribonucleoprotein structures. Methods Enzymol 180: 212-227.
33. Kurland CG, Hughes D, Ehrenberg M. 1996. Limitations of translational accuracy. In Escherichia coli and Salmonella: Cellular and molecular biology (eds. FC Neidhardt et al.), pp. 979-1004. American Society for Microbiology, Washington, DC.
34. Larkin MA, Blackshields G, Brown NP, Chenna R, McGettigan PA, McWilliam H, Valentin F, Wallace IM, Wilm A, Lopez R, et al. 2007. Clustal W and Clustal X version 2.0. Bioinformatics 23: 2947-2948.
35. Laskowski RA, MacArthur MW, Moss DS, Thornton JM. 1993. Procheck - a program to check the stereochemical quality of protein structures. J Appl Crystallogr 26: 283-291.
36. Mallick P, Boutz DR, Eisenberg D, Yeates TO. 2002. Genomic evidence that the intracellular proteins of archaeal microbes contain disulfide bonds. Proc Natl Acad Sci 99: 9679-9684.
37. Marti-Renom MA, Stuart AC, Fiser A, Sanchez R, Melo F, Sali A. 2000. Comparative protein structure modeling of genes and genomes. Annu Rev Biophys Biomol Struct 29: 291-325.
38. McCoy AJ, Grosse-Kunstleve RW, Adams PD, Winn MD, Storoni LC, Read RJ. 2007. Phaser crystallographic software. J Appl Crystallogr 40: 658-674.
39. Merryman C, Noller HF. 1998. Footprinting and modificationinterference analysis of binding sites on RNA. In RNA:protein interactions. A practical approach (ed. CJW Smith), pp. 237-253. IRL Press, Oxford, UK.
40. Murray H, Errington J. 2008. Dynamic control of the DNA replication initiation protein DnaA by Soj/ParA. Cell 135: 74-84.
41. Murshudov GN, Vagin AA, Dodson EJ. 1997. Refinement of macromolecular structures by the maximum-likelihood method. Acta Crystallogr D Biol Crystallogr 53: 240-255.
42. Nishimura K, Hosaka T, Tokuyama S, Okamoto S, Ochi K. 2007a. Mutations in rsmG, encoding a 16S rRNA methyltransferase, result in low-level streptomycin resistance and antibiotic overproduction in Streptomyces coelicolor A3(2). J Bacteriol 189: 3876-3883.
43. Nishimura K, Johansen SK, Inaoka T, Hosaka T, Tokuyama S, Tahara Y, Okamoto S, Kawamura F, Douthwaite S, Ochi K. 2007b. Identification of the RsmG methyltransferase target as 16S rRNA nucleotide G527 and characterization of Bacillus subtilis rsmG mutants. J Bacteriol 189: 6068-6073.
44. 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.
45. Oshima T, Imahori K. 1974. Description of Thermus thermophilus (Yoshida and Oshima), comb. nov., a nonsporulating thermophilic bacterium from a Japanese thermal spa. Int J Syst Bacteriol 24: 102-112.
46. Otwinowski Z, Minor W. 1997. Processing of X-ray diffraction data collected in oscillation mode. Methods Enzymol 276: 307-326.
47. Painter J, Merritt EA. 2006. TLSMD web server for the generation of multi-group TLS models. J Appl Crystallogr 39: 109-111.
48. Peattie DA. 1979. Direct chemical method for sequencing RNA. Proc Natl Acad Sci 76: 1760-1764.
49. Romanowski MJ, Bonanno JB, Burley SK. 2002. Crystal structure of the Escherichia coli glucose-inhibited division protein B (GidB) reveals a methyltransferase fold. Proteins 47: 563-567.
50. Shatsky M, Nussinov R, Wolfson HJ. 2004. A method for simultaneous alignment of multiple protein structures. Proteins 56: 143-156.
51. Shatsky M, Nussinov R, Wolfson HJ. 2006. Optimization of multiple-sequence alignment based on multiple-structure alignment. Proteins 62: 209-217.
52. Shigi N, Sakaguchi Y, Suzuki T, Watanabe K. 2006. Identification of two tRNA thiolation genes required for cell growth at extremely high temperatures. J Biol Chem 281: 14296-14306.
53. Thompson J, Dahlberg AE. 2004. Testing the conservation of the translational machinery over evolution in diverse environments: Assaying Thermus thermophilus ribosomes and initiation factors in a coupled transcription-translation system from Escherichia coli. Nucleic Acids Res 32: 5954-5961.
54. Wimberly BT, Brodersen DE, Clemons WM, Morgan-Warren RJ, Carter AP, Vonrhein C, Hartsch T, Ramakrishnan V. 2000. Structure of the 30S ribosomal subunit. Nature 407: 327-339.
55. Zueva VS, Mankin AS, Bogdanov AA, Baratova LA. 1985. Specific fragmentation of tRNA and rRNA at a 7-methylguanine residue in the presence of methylated carrier RNA. Eur J Biochem 146: 679-687.