Formation of Thiolated Nucleosides Present in tRNA from Salmonella enterica serovar Typhimurium Occurs in Two Principally Distinct Pathways

Journal of Bacteriology

Volumn 186, Issue 3, 2004, Pages 758-766

  Leipuviene, Ramune ^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

2 THIOCYTIDINE; 4 THIOURIDINE; 5 CARBOXYMETHYLAMINOMETHYL 2 THIOURIDINE; 5 METHYLAMINOMETHYL 2 THIOURIDINE; 6 N (4 HYDROXYISOPENTENYL) 2 METHYLTHIOADENOSINE; CYSTATHIONINE GAMMA LYASE; IRON SULFUR PROTEIN; NUCLEOSIDE; TRANSFER RNA; UNCLASSIFIED DRUG;

AMINO ACID SUBSTITUTION; ARTICLE; BACTERIAL GENE; CONTROLLED STUDY; FDX GENE; GENE CLUSTER; GENE DELETION; GENE MUTATION; GENETIC CODE; HSCA GENE; ISCS GENE; ISCU GENE; MOLECULAR DYNAMICS; MOLECULAR MECHANICS; NONHUMAN; OPERON; PRIORITY JOURNAL; PROTEIN TRANSPORT; SALMONELLA ENTERICA; SALMONELLA TYPHIMURIUM;

ESCHERICHIA COLI PROTEINS; HSP70 HEAT-SHOCK PROTEINS; IRON-SULFUR PROTEINS; MUTATION; NUCLEOSIDES; OPERON; RNA, BACTERIAL; RNA, TRANSFER; SALMONELLA TYPHIMURIUM; SULFHYDRYL COMPOUNDS; THIOURIDINE;

BACTERIA (MICROORGANISMS); NEGIBACTERIA; SALMONELLA; SALMONELLA ENTERICA; SALMONELLA ENTERICA SUBSP. ENTERICA SEROVAR TYPHIMURIUM; SALMONELLA TYPHIMURIUM;

EID: 1642541001     PISSN: 00219193     EISSN: None     Source Type: Journal    
DOI: 10.1128/JB.186.3.758-766.2004     Document Type: Article

References (70)

1. Agar, J. N., C. Krebs, J. Frazzon, B. H. Huynh, D. R. Dean, and M. K. Johnson. 2000. IscU as a scaffold for iron-sulfur cluster biosynthesis: sequential assembly of [2Fe-2S] and [4Fe-4S] clusters in IscU. Biochemistry 39:7856-7862.
2. Agris, P., H. Sierzputowska-Gracz, W. Smith, A. Malkiewicz, E. Sochacka, and B. Nawrot. 1992. Thiolation of uridine carbon-2 restricts the motional dynamics of the transfer RNA wobble position nucleoside. J. Am. Chem. Soc. 114:2652-2656.
3. Ajitkumar, P., and J. D. Cherayil. 1988. Thionucleosides in transfer ribonucleic acid: diversity, structure, biosynthesis, and function. Microbiol. Rev. 52:103-113.
4. 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.
5. Arg and their effects on the translation of MS2 RNA. Eur. J. Biochem. 152:645-649.
6. Beinert, H. 2000. Iron-sulfur proteins: ancient structures, still full of surprises. J. Biol. Inorg. Chem. 5:2-15.
7. Beinert, H., R. H. Holm, and E. Münck. 1997. Iron-sulfur clusters: nature's modular, multipurpose structures. Science 277:653-659.
8. Beinert, H., and P. J. Kiley. 1999. Fe-S proteins in sensing and regulatory functions. Curr. Opin. Chem. Biol. 3:152-157.
9. Björk G. R. 1992. The role of modified nucleosides in tRNA interactions, p. 23-85. In D. L. Hatfield, B. J. Lee, and R. M. Pirtle (ed.), Transfer RNA in protein synthesis. CRC Press, Inc., Boca Raton, Fla.
10. Cheek, J., and J. B. Broderick. 2001. Adenosylmethionine-dependent iron-sulfur enzymes: versatile clusters in a radical new role. J. Biol. Inorg. Chem. 6:209-226.
11. 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.
12. 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.
13. Emilsson, V., and C. G. Kurland. 1990. Growth rate dependence of transfer RNA abundance in Escherichia coli. EMBO J. 9:4359-4366.
14. Emilsson, V., A.K., Näslund, and C. G. Kurland. 1992. Thiolation of transfer RNA in Escherichia coli varies with growth rate. Nucleic Acids Res. 20:4499-4505.
15. 6A) present next to the anticodon contributes to the decoding efficiency of the tRNA. J. Bacteriol. 177:1967-1975.
16. Esberg, B., H. C. Leung, H. C. Tsui, G. R. Björk, M. E. Winkler. 1999. Identification of the miaB gene, involved in methylthiolation of isopentenylated A37 derivatives in the tRNA of Salmonella typhimurium and Escherichia coli. J. Bacteriol. 181:7256-7265.
17. 1. Biochem. Biophys. Res. Commun. 37:266-271.
18. Fontecave, M., E. Mulliez, and S. Ollagnier-de-Choudens. 2001. Adenosylmethionine as a source of 5′-deoxyadenosyl radicals. Curr. Opin. Chem. Biol. 5:506-511.
19. Frazzon, J., J. R. Fick, and D. R. Dean. 2002. Biosynthesis of iron-sulphur clusters is a complex and highly conserved process. Biochem. Soc. Trans. 30:680-685.
20. Garland, S. A., K. Hoff, L. E. Vickery, and V. C. Culotta. 1999. Saccharomyces cerevisiae ISU1 and ISU2: members of a well-conserved gene family for iron-sulfur cluster assembly. J. Mol. Biol. 294:897-907.
21. 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.
22. 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.
23. Hagervall, T. G., C. G. Edmonds, J. A. McCloskey, and G. R. Björk. 1987. Transfer RNA(5-methylaminomethyl-2-thiouridine)-methyltransferase from Escherichia coli K-12 has two enzymatic activities. J. Biol. Chem. 262:8488-8495.
24. Hoff, K. G., D. T. Ta, T. L. Tapley, J. J. Silberg, and L. E. Vickery. 2002. Hsc66 substrate specificity is directed toward a discrete region of the iron-sulfur cluster template protein IscU. J. Biol. Chem. 277:27353-27359.
25. 2-Cys motif present in the TtcA protein is required for the thiolation of cytidine in position 32 of tRNA from Salmonella enterica serovar Typhimurium. J. Bacteriol. 186:750-757.
26. Jensen, L. T., and V. C. Culotta. 2000. Role of Saccharomyces cerevisiae ISA1 and ISA2 in iron homeostasis. Mol. Cell. Biol. 20:3918-3927.
27. 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.
28. 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.
29. Kato, S., H. Mihara, T. Kurihara, Y. Takahashi, U. Tokumoto, T. Yoshimura, and N. Esaki. 2002. Cys-328 of IscS and Cys-63 of IscU are the sites of disulfide bridge formation in a covalently bound IscS/IscU complex: implications for the mechanism of iron-sulfur cluster assembly. Proc. Natl. Acad. Sci. USA 99:5948-5952.
30. Kaut, A., H. Lange, K. Diekert, G. Kispal, and R. Lill. 2000. Isalp is a component of the mitochondrial machinery for maturation of cellular iron-sulfur proteins and requires conserved cysteine residues for function. J. Biol. Chem. 275:15955-15961.
31. Kiley, P. J., and H. Beinert. 2003. The role of Fe-S proteins in sensing and regulation in bacteria. Curr. Opin. Microbiol. 6:181-185.
32. Krebs, C., J. N. Agar, A. D. Smith, J. Frazzon, D. R. Dean, B. H. Huynh, and M. K. Johnson. 2001. IscA, an alternate scaffold for Fe-S cluster biosynthesis. Biochemistry 40:14069-14080.
33. Lauhon, C. T. 2002. Requirement for IscS in biosynthesis of all thionucleosides in Escherichia coli. J. Bacteriol. 184:6820-6829.
34. Lauhon, C. T., and R. Kambampati. 2000. The iscS gene in Escherichia coli is required for the biosynthesis of 4-thiouridine, thiamine, and NAD. J. Biol. Chem. 275:20096-20103.
35. Leung, H. C. E., Y. Q. Chen, and M. E. Winkler. 1997. Regulation of substrate recognition by the MiaA tRNA prenyltransferase modification enzyme of Escherichia coli K-12. J. Biol. Chem. 272:13073-13083.
36. Li, J. N., B. Esberg, J. F. Curran, and G. R. Björk. 1997. Three modified nucleosides present in the anticodon stem and loop influence the in vivo aa-tRNA selection in a tRNA-dependent manner. J. Mol. Biol. 271:209-221.
37. Madore, E., C. Florentz, R. Giege, S. Sekine, S. Yokoyama, and J. Lapointe. 1999. Effect of modified nucleotides on Escherichia coli tRNA(Glu) structure and on its aminoacylation by glutamyl-tRNA synthetase-predominant and distinct roles of the mnm(5) and s(2) modifications of U34. Eur. J. Biochem. 266:1128-1135.
38. Marquet, A. 2001. Enzymology of carbon-sulfur bond formation. Curr. Opin. Chem. Biol. 5:541-549.
39. Marquet, A., B. T. Bui, and D. Florentin. 2001. Biosynthesis of biotin and lipoic acid. Vitam. Horm. 61:51-101.
40. McCloskey, J. A., D. E. Graham, S. Zhou, P. F. Crain, M. Ibba, J. Konisky, D. Söll, and G. J. Olsen. 2001. Post-transcriptional modification in archaeal tRNAs: identities and phylogenetic relations of nucleotides from mesophilic and hyperthermophilic Methanococcales. Nucleic Acids Res. 29:4699-4706.
41. Moore, J. A., and C. D. Poulter. 1997. Escherichia coli dimethylallyl diphosphate: tRNA dimethylallyltransferase: a binding mechanism for recombinant enzyme. Biochemistry 36:604-614.
42. Mueller, E. G., P. M. Palenchar, and C. J. Buck. 2001. The role of the cysteine residues of ThiI in the generation of 4-thiouridine in tRNA. J. Biol. Chem. 276:33588-33595.
43. 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.
44. 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.
45. Ollagnier-de-Choudens, S., T. Mattioli, Y. Takahashi, and M. Fontecave. 2001. Iron-sulfur cluster assembly: characterization of IscA and evidence for a specific and functional complex with ferredoxin. J. Biol. Chem. 276:22604-22607.
46. Ollagnier-de Choudens, S., L. Nachin, Y. Sanakis, L. Loiseau, F. Barras, and M. Fontecave. 2003. SufA from Erwinia chrysanthemi. Characterization of a scaffold protein required for iron-sulfur cluster assembly. J. Biol. Chem. 278:17993-18001.
47. 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.
48. Pelzer, W., U. Mühlenhoff, K. Diekert, K. Siegmund, G. Kispal, and R. Lill. 2000. Mitochondrial Isa2p plays a crucial role in the maturation of cellular iron-sulfur proteins. FEBS Lett. 476:134-139.
49. Persson, B. C., and G. R. Björk. 1993. Isolation of the gene (miaE) encoding the hydroxylase involved in the synthesis of 2-methylthio-cis-ribozeatin in tRNA of Salmonella typhimurium and characterization of mutants. J. Bacteriol. 175:7776-7785.
50. 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.
51. Pro GGG of Salmonella typhimurium. J. Mol. Biol. 266:283-296.
52. 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.
53. Ramabhadran, T. V., and J. Jagger. 1976. Mechanism of growth delay induced in Escherichia coli by near ultraviolet radiation. Proc. Natl. Acad. Sci. USA 73:59-63.
54. Rosenbaum, N., and M. L. Gefter. 1972. Delta 2-isopentenylpyrophosphate: transfer ribonucleic acid 2-isopentenyltransferase from Escherichia coli. Purification and properties of the enzyme. J. Biol. Chem. 247:5675-5680.
55. Rozenski, J., P. F. Crain, and J. A. McCloskey. 1999. The RNA modification database: 1999 update. Nucleic Acids Res. 27:196-197.
56. Schmieger, H. 1972. Phage P22-mutants with increased or decreased transduction abilities. Mol. Gen. Genet. 119:75-88.
57. Schwartz, C. J., J. L. Giel, T. Patschkowski, C. Luther, F. J. Ruzicka, H. Beinert, and P. J. Kiley. 2001. IscR, an Fe-S cluster-containing transcription factor, represses expression of Escherichia coli genes encoding Fe-S cluster assembly proteins. Proc. Natl. Acad. Sci. USA 98:14895-14900.
58. Skovran, E., and D. M. Downs. 2000. Metabolic defects caused by mutations in the isc gene cluster in Salmonella enterica serovar Typhimurium: Implications for thiamine synthesis. J. Bacteriol. 182:3896-3903.
59. Smith, A. D., J. N. Agar, K. A. Johnson, J. Frazzon, I. J. Amster, D. R. Dean, and M. K. Johnson. 2001. Sulfur transfer from IscS to IscU: the first step in iron-sulfur cluster biosynthesis. J. Am. Chem. Soc. 123:11103-11104.
60. 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.
61. Glu is a positive determinant for aminoacylation by Escherichia coli glutamyl-tRNA synthetase. Biochemistry 32:3836-3841.
62. Takahashi, Y., and M. Nakamura. 1999. Functional assignment of the ORF2-iscS-iscU-iscA-hscB-hscA-fdx-ORF3 gene cluster involved in the assembly of Fe-S clusters in Escherichia coli. J. Biochem. (Tokyo) 126:917-926.
63. Taylor, S. V., N. L. Kelleher, C. Kinsland, H. J. Chiu, C. K. Costello, A. D. Backstrom, F. W. McLafferty, and T. P. Begley. 1998. Thiamin biosynthesis in Escherichia coli-identification of this thiocarboxylate as the immediate sulfur donor in the thiazole formation. J. Biol. Chem. 273:16555-16560.
64. Thomas, G., and A. Favre. 1975. 4-Thiouridine as the target for near-ultraviolet light induced growth delay in Escherichia coli. Biochem. Biophys. Res. Commun. 66:1454-1461.
65. Tokumoto, U., and Y. Takahashi. 2001. Genetic analysis of the isc operon in Escherichia coli involved in the biogenesis of cellular iron-sulfur proteins. J. Biochem. (Tokyo) 130:63-71.
66. Urbina, H. D., J. J. Silberg, K. G. Hoff, and L. E. Vickery. 2001. Transfer of sulfur from IscS to IscU during Fe/S cluster assembly. J. Biol. Chem. 276:44521-44526.
67. 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.
68. Webb, E., K. Claas, and D. M. Downs. 1997. Characterization of thiI, a new gene involved in thiazole biosynthesis in Salmonella typhimurium. J. Bacteriol. 179:4399-4402.
69. Yokoyama, S., T. Watanabe, K. Murao, H. Ishikura, Z. Yamaizumi, S. Nishimura, and T. Miyazawa. 1985. Molecular mechanism of codon recognition by tRNA species with modified uridine in the first position of the anticodon. Proc. Natl. Acad. Sci. USA 82:4905-4909.
70. Yuvaniyama, P., J. N. Agar, V. L. Cash, M. K. Johnson, and D. R. Dean. 2000. NifS-directed assembly of a transient [2Fe-2S] cluster within the NifU protein. Proc. Natl. Acad. Sci. USA 97:599-604.