The Conserved Cys-X1-X2-Cys Motif Present in the TtcA Protein Is Required for the Thiolation of Cytidine in Position 32 of tRNA from Salmonella enterica serovar Typhimurium

Journal of Bacteriology

Volumn 186, Issue 3, 2004, Pages 750-757

  Jäger, Gunilla ^a   Leipuviene, Ramune ^a   Pollard, Michael G ^a   Qian, Qiang ^a,b   Björk, Glenn R ^a  

^a UMEÅ UNIVERSITY   (Sweden)

^b Telecommunication System Inc   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CYTIDINE; TRANSFER RNA; ARGININE; BACTERIAL PROTEIN; BACTERIAL RNA; SULFUR; THIOL DERIVATIVE;

AMINO TERMINAL SEQUENCE; ANTICODON; ARTICLE; CONGENIC STRAIN; CONTROLLED STUDY; FRAMESHIFT MUTATION; GENE DELETION; GENOTYPE; GROWTH RATE AND GROWTH REGULATION; MOLECULAR MECHANICS; NONHUMAN; PRIORITY JOURNAL; PROTEIN MOTIF; RNA TRANSLATION; SALMONELLA ENTERICA; SALMONELLA TYPHIMURIUM; SEQUENCE ANALYSIS; CHEMISTRY; CODON; GENETICS; METABOLISM; NUCLEOTIDE SEQUENCE; OXIDATION REDUCTION REACTION; PHYSIOLOGY; PROTEIN SYNTHESIS;

ANIMALIA; ARCHAEA; ESCHERICHIA COLI; NEGIBACTERIA; SALMONELLA; SALMONELLA ENTERICA; SALMONELLA ENTERICA SUBSP. ENTERICA SEROVAR TYPHIMURIUM; SALMONELLA TYPHIMURIUM;

AMINO ACID MOTIFS; ARGININE; BACTERIAL PROTEINS; CODON; CONSERVED SEQUENCE; CYTIDINE; OXIDATION-REDUCTION; PROTEIN BIOSYNTHESIS; RNA, BACTERIAL; RNA, TRANSFER; SALMONELLA TYPHIMURIUM; SULFHYDRYL COMPOUNDS; SULFUR;

EID: 1342307414     PISSN: 00219193     EISSN: None     Source Type: Journal    
DOI: 10.1128/JB.186.3.750-757.2004     Document Type: Article

References (57)

1. Ajitkumar, P., and J. D. Cherayil. 1988. Thionucleosides in transfer ribonucleic acid: diversity, structure, biosynthesis, and function. Microbiol. Rev. 52:103-113.
2. Auffinger, P., and E. Westhof. 1998. Location and distribution of modified nucleotides in tRNA, p. 569-576. In H. Grosjean and R. Benne (ed.), Modification and editing of RNA. ASM Press, Washington, D.C.
3. Auffinger, P., and E. Westhof. 1999. Singly and bifurcated hydrogen-bonded base-pairs in tRNA anticodon hairpins and ribozymes. J. Mol. Biol. 292:467-483.
4. Avital, S., and D. Elson. 1969. A convenient procedure for preparing transfer ribonucleic acid from Escherichia coli. Biochim. Biophys. Acta 179:297-307.
5. Arg and their effects on the translation of MS2 RNA. Eur. J. Biochem. 152:645-649.
6. Bertani, G. 1951. Studies on lysogenesis. J. Bacteriol. 62:293-300.
7. Björk, G. R. 1980. A novel link between the biosynthesis of aromatic amino acids and transfer RNA modification in Escherichia coli. J. Mol. Biol. 140:391-410.
8. Björk, G. R. 1995. Genetic dissection of synthesis and function of modified nucleosides in bacterial transfer RNA. Prog. Nucleic Acid Res. Mol. Biol. 50:263-338.
9. Bochner, B. R., and M. A. Savageau. 1977. Generalized indicator plate for genetic, metabolic, and taxonomic studies with microorganisms. Appl. Environ. Microbiol. 33:434-444.
10. Cortese, R., R. Landsberg, R. A. Haar, H. E. Umbarger, and B. N. Ames. 1974. Pleiotropy of hisT mutants blocked in pseudouridine synthesis in tRNA: leucine and isoleucine-valine operons. Proc. Natl. Acad. Sci. USA 71:1857-1861.
11. Curran, J. F. 1993. Analysis of effects of tRNA: message stability on frameshift frequency at the Escherichia coli RF2 programmed frameshift site. Nucleic Acids Res. 21:1837-1843.
12. Curran, J. F. 1995. Decoding with the A-I wobble pair is inefficient. Nucleic Acids Res. 23:683-688.
13. Curran, J. F., and M. Yarus. 1989. Rates of aminoacyl-tRNA selection at 29 sense codons in vivo. J. Mol. Biol. 209:65-77.
14. Cusack, S., A. Yaremchuk, I. Krikliviy, and M. Tukalo. 1998. tRNA(Pro) anticodon recognition by Thermus thermophilus prolyl-tRNA synthetase. Structure 6:101-108.
15. Cusack, S., A. Yaremchuk, and M. Tukalo. 1996. The crystal structures of T. thermophilus lysyl-tRNA synthetase complexed with E. coli tRNA(Lys) and a T. thermophilus tRNA(Lys) transcript: anticodon recognition and conformational changes upon binding of a lysyl-adenylate analogue. EMBO J. 15:6321-6334.
16. Datsenko, K. A., and B. L. Wanner. 2000. One-step inactivation of chromosomal genes in Escherichia coli K-12 using PCR products. Proc. Natl. Acad. Sci. USA 97:6640-6645.
17. Davis, W., D. Botstein, and J. R. Roth. 1980. A manual for genetic engineering: advanced bacterial genetics. Cold Spring Harbor Laboratory, Cold Spring Harbor, N.Y.
18. Donohue, J. 1969. On N-H-S hydrogen bonds. J. Mol. Biol. 45:231-235.
19. Ehrenberg, M., and C. G. Kurland. 1984. Costs of accuracy determined by a maximal growth rate constraint. Q. Rev. Biophys. 17:45-82.
20. Emilsson, V., and C. G. Kurland. 1990. Growth rate dependence of transfer RNA abundance in Escherichia coli. EMBO J. 9:4359-4366.
21. Ericsson, J. U., and G. R. Björk. 1986. Pleiotropic effects induced by modification deficiency next to the anticodon of tRNA from Salmonella typhimurium LT2. J. Bacteriol. 166:1013-1021.
22. 6A) present next to the anticodon contributes to the decoding efficiency of the tRNA. J. Bacteriol. 177:1967-1975.
23. Gehrke, C. W., and K. C. Kuo. 1990. Ribonucleoside analysis by reversed-phase high performance liquid chromatography, p. A3-A71. In C. W. Gehrke and K. C. T. Kuo (ed.), Chromatography and modification of nucleosides. A. Analytical methods for major and modified nucleosides. Journal of Chromatography Library. Elsevier, Amsterdam, The Netherlands.
24. Gehrke, C. W., K. C. Kuo, R. A. McCune, K. O. Gerhardt, and P. F. Agris. 1982. Quantitative enzymatic hydrolysis of tRNAs: reversed-phase high-performance liquid chromatography of tRNA nucleosides. J. Chromatogr. 230:297-308.
25. Hagervall, T. G., T. M. Tuohy, J. F. Atkins, and G. R. Björk. 1993. Deficiency of 1-methylguanosine in tRNA from Salmonella typhimurium induces frameshifting by quadruplet translocation. J. Mol. Biol. 232:756-765.
26. Kambampati, R., and C. T. Lauhon. 2000. Evidence for the transfer of sulfane sulfur from IscS to ThiI during the in vitro biosynthesis of 4-thiouridine in Escherichia coli tRNA. J. Biol. Chem. 275:10727-10730.
27. Kambampati, R., and C. T. Lauhon. 2003. MnmA and IscS are required for in vitro 2-thiouridine biosynthesis in Escherichia coli. Biochemistry 42:1109-1117.
28. Kruse, T. A., B. F. Clark, and M. Sprinzl. 1978. The effect of specific structural modification on the biological activity of E. coli arginine tRNA. Nucleic Acids Res. 5:879-892.
29. Lauhon, C. T. 2002. Requirement for IscS in biosynthesis of all thionucleosides in Escherichia coli. J. Bacteriol. 184:6820-6829.
30. a. Leipuviene, R., Q. Qion, and G. R. Björk. 2004. Formation of thiolated nucleosides present in tRNA from Salmonella enterica serovar Typhimurium occurs in distinct pathways. J. Bacteriol. 186:768-776.
31. Li, J. N., and G. R. Björk. 1995. 1-Methylguanosine deficiency of tRNA influences cognate codon interaction and metabolism in Salmonella typhimurium. J. Bacteriol. 177:6593-6600.
32. Link, A. J., D. Phillips, and G. M. Church. 1997. Methods for generating precise deletions and insertions in the genome of wild-type Escherichia coli: application to open reading frame characterization. J. Bacteriol. 179:6228-6237.
33. McCloskey, J. A., D. E. Graham, S. Zhou, P. F. Crain, M. Ibba, J. Konisky, D. Soll, and G. J. Olsen. 2001. Post-transcriptional modification in archaeal tRNAs: identities and phylogenetic relations of nucleotides from mesophilie and hyperthermophilic Methanococcales. Nucleic Acids Res. 29:4699-4706.
34. Miller J. H. 1972. Experiments in molecular genetics. Cold Spring Harbor Laboratory, Cold Spring Harbor, N.Y.
35. Milton, D. L., R. O'Toole, P. Horstedt, and H. Wolf-Watz. 1996. Flagellin A is essential for the virulence of Vibrio anguillarum. J. Bacteriol. 178:1310-1319.
36. Neidhardt, F. C., P. L. Bloch, S. Pedersen, and S. Reeh. 1977. Chemical measurement of steady-state levels of ten aminoacyl-transfer ribonucleic acid synthetases in Escherichia coli. J. Bacteriol. 129:378-387.
37. Neidhardt, F. C., P. L. Bloch, and D. F. Smith. 1974. Culture medium for enterobacteria. J. Bacteriol. 119:736-747.
38. Nilsson, K., H. K. Lundgren, T. G. Hagervall, and G. R. Björk. 2002. The cysteine desulfurase IscS is required for synthesis of all five thiolated nucleosides present in tRNA from Salmonella enterica serovar Typhimurium. J. Bacteriol. 184:6830-6835.
39. Palenchar, P. M., C. J. Buck, H. Cheng, T. J. Larson, and E. G. Mueller. 2000. Evidence that ThiI, an enzyme shared between thiamine and 4-thiouridine biosynthesis, may be a sulfurtransferase that proceeds through a persulfide intermediate. J. Biol. Chem. 275:8283-8286.
40. Pierrel, F., G. R. Björk, M. Fontecave, and M. Atta. 2002. Enzymatic modification of tRNAs: MiaB is an iron-sulfur protein. J. Biol. Chem. 277:13367-13370.
41. Pomerantz, S. C., and J. A. McCloskey. 1990. Analysis of RNA hydrolyzates by liquid chromatography-mass spectrometry. Methods Enzymol. 193:796-824.
42. Pro of Salmonella typhimurium induce + 1 frameshifting at the peptidyl-site. J. Mol. Biol. 273:978-992.
43. Qian, Q., J. N. Li, H. Zhao, T. G. Hagervall, P. J. Farabaugh, and G. R. Björk. 1998. A new model for phenotypic suppression of frameshift mutations by mutant tRNAs. Mol. Cell 1:471-482.
44. 6-threonylcarbamoyladenosine in tRNA of Escherichia coli modestly improves the efficiency of the tRNA. J. Bacteriol. 180:1808-1813.
45. Quigley, G. J., and A. Rich. 1976. Structural domains of transfer RNA molecules. Science 194:796-806.
46. Rould, M. A., J. J. Perona, and T. A. Steitz. 1991. Structural basis of anticodon loop recognition by glutaminyl-tRNA synthetase. Nature 352:213-218.
47. Ruff, M., S. Krishnaswamy, M. Boeglin, A. Poterszman, A. Mitschler, A. Podjarny, B. Rees, J. C. Thierry, and D. Moras. 1991. Class II aminoacyl transfer RNA synthetases: crystal structure of yeast aspartyl-tRNA synthetase complexed with tRNA(Asp). Science 252:1682-1689.
48. Schmieger, H. 1972. Phage P22-mutants with increased or decreased transduction abilities. Mol. Gen. Genet. 119:75-88.
49. Singer, M., T. A. Baker, G. Schnitzler, S. M. Deischel, M. Goel, W. Dove, K. J. Jaacks, A. D. Grossman, J. W. Erickson, and C. A. Gross. 1989. A collection of strains containing genetically linked alternating antibiotic resistance elements for genetic mapping of Escherichia coli. Microbiol. Rev. 53:1-24.
50. Smith, D., and M. Yarus. 1989. tRNA-tRNA interactions within cellular ribosomes. Proc. Natl. Acad. Sci. USA 86:4397-4401.
51. Sofia, H. J., G. Chen, B. G. Hetzler, J. F. ReyesSpindola, and N. E. Miller. 2001. Radical SAM, a novel protein superfamily linking unresolved steps in familiar biosynthetic pathways with radical mechanisms: functional characterization using new analysis and information visualization methods. Nucleic Acids Res. 29:1097-1106.
52. Soma, A., Y. Ikeuchi, S. Kanemasa, K. Kobayashi, N. Ogasawara, T. Ote, J. Kato, K. Watanabe, Y. Sekine, and T. Suzuki. 2003. An RNA-modifying enzyme that governs both the codon and amino acid specificities of isoleucine tRNA. Mol. Cell 12:689-698.
53. Sprinzl, M., and K. S. Vassilenko. 2003. tRNA sequences and tRNA genes database. [Online] http://www.uni-bayreuth.de/departments/biochimie/sprinzl/trna/.
54. Sullivan, M. A., J. F. Cannon, F. H. Webb, and R. M. Bock. 1985. Antisuppressor mutation in Escherichia coli defective in biosynthesis of 5-methylaminomethyl-2-thiouridine. J. Bacteriol. 161:368-376.
55. Urbonavicius, J., Q. Qian, J. M. Durand, T. G. Hagervall, and G. R. Björk. 2001. Improvement of reading frame maintenance is a common function for several tRNA modifications. EMBO J. 20:4863-4873.
56. Vogel, H. J., and D. M. Bonner. 1956. Acetylornithinase of Escherichia coli: Partial purification and some properties. J. Biol. Chem. 218:97-106.
57. Westhof, E., P. Dumas, and D. Moras. 1985. Crystallographic refinement of yeast aspartic acid transfer RNA. J. Mol. Biol. 184:119-145.