Role of 16S ribosomal RNA methylations in translation initiation in Escherichia coli

EMBO Journal

Volumn 27, Issue 6, 2008, Pages 840-851

  Das, Gautam ^a   Thotala, Dinesh Kumar ^a   Kapoor, Suman ^a   Karunanithi, Sheelarani ^a   Thakur, Suman S ^a   Singh, N Sadananda ^a   Varshney, Umesh ^a  

^a INDIAN INSTITUTE OF SCIENCE   (India)

Author keywords

5,10 methylene tetrahydrofolate dehydrogenase; folD; Methyltransferase; Modified nucleoside; S adenosyl L methionine

Indexed keywords

FORMYLMETHIONYL TRANSFER RIBONUCLEIC ACID; METHIONINE; METHYLTRANSFERASE; RNA 16S; S ADENOSYLMETHIONINE; TRANSFER RNA; UNCLASSIFIED DRUG;

ANTICODON; ARTICLE; BACTERIAL GENE; BACTERIAL STRAIN; BACTERIUM ISOLATION; BASE PAIRING; CONTROLLED STUDY; ESCHERICHIA COLI; FOLD GENE; GENE MUTATION; GENETIC SCREENING; MATRIX ASSISTED LASER DESORPTION IONIZATION TIME OF FLIGHT MASS SPECTROMETRY; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN PROTEIN INTERACTION; PROTEIN STRUCTURE; RNA METHYLATION; RNA SEQUENCE; SUPPRESSOR GENE; TRANSLATION INITIATION;

5,10-METHYLENETETRAHYDROFOLATE REDUCTASE (FADH2); AMINO ACID SUBSTITUTION; BASE SEQUENCE; ESCHERICHIA COLI PROTEINS; METHYLATION; MOLECULAR SEQUENCE DATA; MUTATION; PEPTIDE CHAIN INITIATION, TRANSLATIONAL; RIBOSOMES; RNA, BACTERIAL; RNA, RIBOSOMAL, 16S; RNA, TRANSFER, MET;

ESCHERICHIA COLI;

EID: 40949093636     PISSN: 02614189     EISSN: 14602075     Source Type: Journal    
DOI: 10.1038/emboj.2008.20     Document Type: Article

References (48)

1. Alimchandani HR, Sreenivasan A (1957) Inactivity of pteroylglutamic acid and leucovorin in overcoming sulfonamide growth inhibition of Escherichia coli. J Bacteriol 74: 171-174
2. 5C methyltransferase specific for 16 S rRNA nucleotide 1407. J Mol Biol 359: 777-786
3. Antoun A, Pavlov MY, Lovmar M, Ehrenberg M (2006) How initiation factors maximize the accuracy of tRNA selection in initiation of bacterial protein synthesis. Mol Cell 23: 183-193
4. Basturea GN, Rudd KE, Deutscher MP (2006) Identification and characterization of RsmE, the founding member of a new RNA base methyltransferase family. RNA 12: 426-434
5. Brimacombe R, Mitchell P, Osswald M, Stade K, Bochkariov D (1993) Clustering of modified nucleotides at the functional center of bacterial ribosomal RNA. FASEB J 7: 161-167
6. Dallas A, Noller HF (2001) Interaction of translation initiation factor 3 with the 30S ribosomal subunit. Mol Cell 8: 855-864
7. Decatur WA, Fournier MJ (2002) rRNA modifications and ribosome function. Trends Biochem Sci 27: 344-351
8. DeLano WL (2002) The PyMOL Molecular Graphics System. Palo Alto, CA, USA: DeLano Scientific (http://www.pymol.org)
9. Guillon JM, Mechulam Y, Schmitter JM, Blanquet S, Fayat G (1992) Disruption of the gene for Met-tRNA(fMet) formyltransferase severely impairs growth of Escherichia coli. J Bacteriol 174: 4294-4301
10. Guymon R, Pomerantz SC, Crain PF, McCloskey JA (2006) Influence of phylogeny on posttranscriptional modification of rRNA in thermophilic prokaryotes: the complete modification map of 16S rRNA of Thermus thermophilus. Biochemistry 45: 4888-4899
11. Hartz D, Binkley J, Hollingsworth T, Gold L (1990) Domains of initiator-tRNA and initiation codon crucial for initiator tRNA selection by Escherichia coli IF3. Genes Dev 4: 1790-1800
12. Hartz D, McPheeters DS, Gold L (1989) Selection of the initiator tRNA by Escherichia coli initiation factors. Genes Dev 3: 1899-1912
13. Helser TL, Davies JE, Dahlberg JE (1972) Mechanism of kasugamycin resistance in Escherichia coli. Nat New Biol 235: 6-9
14. Heus HA, van Kimmenade JMA, van Knippenberg PH (1983) High-resolution proton magnetic resonance studies of the 3′-terminal colicin fragment of 16 S ribosomal RNA from Escherichia coli assignment of iminoproton resonances by nuclear Overhauser effect experiments and the influence of adenine dimethylation on the hairpin conformation. J Mol Biol 170: 939-956
15. Hoang L, Fredrick K, Noller HF (2004) Creating ribosomes with an all-RNA 30S subunit P site. Proc Natl Acad Sci USA 101: 12439-12443
16. Hui A, de Boer HA (1987) Specialized ribosome system: preferential translation of a single mRNA species by a subpopulation of mutated ribosomes in Escherichia coli. Proc Natl Acad Sci USA 84: 4762-4766
17. 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
18. Kirpekar F, Douthwaite S, Roepstorff P (2000) Mapping posttranscriptional modifications in 5S ribosomal RNA by MALDI mass spectrometry. RNA 6: 296-306
19. Korostelev A, Trakhanov S, Laurberg M, Noller HF (2006) Crystal structure of a 70S ribosome-tRNA complex reveals functional interactions and rearrangements. Cell 126: 1065-1077
20. Lancaster L, Noller HF (2005) Involvement of 16S rRNA nucleotides G1338 and A1339 in discrimination of initiator tRNA. Mol Cell 20: 623-632
21. Lee C, Yu D, Velasco M, Tessarollo L, Swing DA, Court DL, Jenkins NA, Copeland NG (2001) A highly efficient Escherichia coli-based chromosome engineering system adapted for recombinogenic targeting and subcloning of BAC DNA. Genomics 73: 56-65
22. Loenen WA (2006) S-Adenosylmethionine: jack of all trades and master of everything? Biochem Soc Trans 34: 330-333
23. Low KB (1968) Formation of merodiploids in matings with a class of Rec-recipient strains of Escherichia coli K12. Proc Natl Acad Sci USA 60: 160-167
24. Mandal N, Mangroo D, Dalluge JJ, McCloskey JA, RajBhandary UL (1996) Role of the three consecutive G:C base pairs conserved in the anticodon stem of initiator tRNAs in initiation of protein synthesis in Escherichia coli. RNA 2: 473-482
25. Marck C, Grosjean H (2002) tRNomics: analysis of tRNA genes from 50 genomes of eukarya, archaea, and bacteria reveals anticodon-sparing strategies and domain-specific features. RNA 8: 1189-1232
26. Matthews RG (1996) One-carbon metabolism. In Cellular and Molecular Biology, Escherichia coli and Salmonella, Neidhardt FC, Curtiss R (eds), Vol. 1, pp 600-611. Washington, DC: Am Soc Microbiol
27. Mayer C, Stortchevoi A, Kohrer C, Varshney U, RajBhandary UL (2001) Initiator tRNA and its role in initiation of protein synthesis. Cold Spring Harb Symp Quant Biol 66: 195-206
28. McCutcheon JP, Agrawal RK, Philips SM, Grassucci RA, Gerchman SE, Clemons Jr WM, Ramakrishnan V, Frank J (1999) Location of translational initiation factor IF3 on the small ribosomal subunit. Proc Natl Acad Sci USA 96: 4301-4306
29. Miller JH (1972) In Experiments in Molecular Genetics. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory
30. Newton DT, Creuzenet C, Mangroo D (1999) Formylation is not essential for initiation of protein synthesis in all eubacteria. J Biol Chem 274: 22143-22146
31. Nilsson AI, Zorzet A, Kanth A, Dahlstrom S, Berg OG, Andersson DI (2006) Reducing the fitness cost of antibiotic resistance by amplification of initiator tRNA genes. Proc Natl Acad Sci USA 103: 6976-6981
32. O'Connor M, Gregory ST, RajBhandary UL, Dahlberg AE (2001) Altered discrimination of start codons and initiator tRNAs by mutant initiation factor 3. RNA 7: 969-978
33. O'Connor M, Thomas CL, Zimmermann RA, Dahlberg AE (1997) Decoding fidelity at the ribosomal A and P sites: influence of mutations in three different regions of the decoding domain in 16S rRNA. Nucleic Acids Res 25: 1185-1193
34. RajBhandary UL, Chow CM (1995) Initiator tRNAs and initiation of protein synthesis. In tRNA: Structure, Biosynthesis, and Function, Soll D, RajBhandary UL (eds), pp 511-528. Washington, DC: American Society for Microbiology
35. RajBhandary UL, Ghosh HP (1969) Studies on polynucleotides XCI yeast methionine transfer ribonucleic acid: purification, properties, and terminal nucleotide sequences. J Biol Chem 244: 1104-1113
36. Rao AR, Varshney U (2002) Characterization of Mycobacterium tuberculosis ribosome recycling factor (RRF) and a mutant lacking six amino acids from the C-terminal end reveals that the C-terminal residues are important for its occupancy on the ribosome. Microbiology 148: 3913-3920
37. Schulman LH, Pelka H (1985) In vitro conversion of a methionine to a glutamine-acceptor tRNA. Biochemistry 24: 7309-7314
38. 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
39. Selmer M, Dunham CM, Murphy IV FV, Weixlbaumer A, Petry S, Kelley AC, Weir JR, Ramakrishnan V (2006) Structure of the 70S ribosome complexed with mRNA and tRNA. Science 313: 1935-1942
40. Singer M, Baker TA, Schnitzler G, Deischel SM, Goel M, Dove W, Jaacks KJ, Grossman AD, Erickson JW, Gross CA (1989) A collection of strains containing genetically linked alternating antibiotic resistance elements for genetic mapping of Escherichia coli. Microbiol Rev 53: 1-24
41. van Buul DPJJ, Visser W, van Knippenberg PH (1984) Increased translational fidelity caused by the antibiotic kasugamycin and ribosomal ambiguity in mutants harbouring the ksgA gene. FEBS Lett 177: 119-124
42. Varshney U, Lee CP, RajBhandary UL (1991) Direct analysis of aminoacylation levels of tRNAs in vivo application to studying recognition of Escherichia coli initiator tRNA mutants by glutaminyl-tRNA synthetase. J Biol Chem 266: 24712-24718
43. Varshney U, Lee CP, RajBhandary UL (1993) From elongator tRNA to initiator tRNA. Proc Natl Acad Sci USA 90: 2305-2309
44. Varshney U, RajBhandary UL (1990) Initiation of protein synthesis from a termination codon. Proc Natl Acad Sci USA 87: 1586-1590
45. Varshney U, Ramesh V, Madabushi A, Gaur R, Subramanya HS, RajBhandary UL (2004) Mycobacterium tuberculosis Rv2118c codes for a single-component homotetrameric m1A58 tRNA methyltransferase. Nucleic Acids Res 32: 1018-1027
46. Wang W, Kramer PM, Yang S, Pereira MA, Tao L (2001) Reversed-phase high-performance liquid chromatography procedure for the simultaneous determination of S-adenosyl-L-methionine, S-adenosyl- L-homocysteine in mouse liver and the effect of methionine on their concentrations. J Chromatogr B Biomed Sci Appl 762: 59-65
47. Wimberly BT, Brodersen DE, Clemons Jr WM, Morgan-Warren RJ, Carter AP, Vonrhein C, Hartsch T, Ramakrishnan V (2000) Structure of the 30S ribosomal subunit. Nature 407: 327-339
48. 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