Requirement for IscS in biosynthesis of all thionucleosides in Escherichia coli

Journal of Bacteriology

Volumn 184, Issue 24, 2002, Pages 6820-6829

  Lauhon, Charles T ^a  

^a UNIVERSITY OF WISCONSIN MADISON   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

2 THIOCYTIDINE; 5 METHYLAMINOMETHYLURIDINE; 6 N DIMETHYL 2 METHYLTHIOADENOSINE; 6 N DIMETHYLADENOSINE; ADENOSINE DERIVATIVE; BACTERIAL PROTEIN; CYSTEINE DERIVATIVE; CYTIDINE DERIVATIVE; MUTANT PROTEIN; NUCLEASE; NUCLEOSIDE DERIVATIVE; PROTEIN CSDA; PROTEIN CSDB; PROTEIN ISCS; SULFUR; TRANSFER RNA; UNCLASSIFIED DRUG; URIDINE DERIVATIVE;

ARTICLE; BACTERIAL CELL; BACTERIAL GROWTH; BACTERIAL STRAIN; CELL ISOLATION; ENZYME METABOLISM; ESCHERICHIA COLI; FRACTIONATION; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; INCUBATION TIME; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN SYNTHESIS; RNA ISOLATION;

CARBON-SULFUR LYASES; CYTIDINE; ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; IRON-SULFUR PROTEINS; RNA, TRANSFER; SULFIDES; THIONUCLEOSIDES;

BACTERIA (MICROORGANISMS); ESCHERICHIA COLI; INSERTION SEQUENCES; NEGIBACTERIA;

EID: 0036952614     PISSN: 00219193     EISSN: None     Source Type: Journal    
DOI: 10.1128/JB.184.24.6820-6829.2002     Document Type: Article

References (47)

1. Ashraf, S. S., E. Sochacka, R. Cain, R. Guenther, A. Malkiewicz, and P. F. Agris. 1999. Single atom modification (O->S) of tRNA confers ribosome binding. RNA 5:188-194.
2. Beinert, H. 2000. A tribute to sulfur. Eur J. Biochem. 18:5657-5664.
3. Bjork, 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.
4. Bjork, G. R., J. U. Ericson, C. E. Gustafsson, T. G. Hagervall, Y. H. Jonsson, and P. M. Wikstrom. 1987. Transfer RNA modification. Annu. Rev. Biochem. 56:263-287.
5. Blondel, M. O., and A. Favre. 1988. tRNAPhe and tRNAPro are the near-ultraviolet molecular targets triggering the growth delay effect. Biochem. Biophys. Res. Commun. 150:979-986.
6. Buck, M., M. Connick, and B. N. Ames. 1983. Complete analysis of tRNA-modified nucleosides by high-performance liquid chromatography: the 29 modified nucleosides of Salmonella typhimurium and Escherichia coli tRNA. Anal. Biochem. 129:1-13.
7. Elseviers, D., L. A. Petrullo, and P. Gallaagher. 1984. Novel E. coli mutants deficient in biosynthesis of 5-methylaminomethyl-2-thiouridine. Nucleic Acids Res. 12:3521-3534.
8. Esberg, B., H. C. E. Leung, H. C. T. Tsui, G. Bjork, and 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.
9. Flint, D. H. 1996. Escherichia coli contains a protein that is homologous in function and N-terminal sequence to the protein encoded by the nifS gene of Azotobacter vinelandii and that can participate in the synthesis of the Fe-S cluster of dihydroxy-acid dehydratase. J. Biol. Chem. 271:16068-16074.
10. Flint, D. H., J. F. Tuminello, and T. J. Miller. 1996. Studies on the synthesis of the Fe-S cluster of dihydroxy-acid dehydratase in Escherichia coli crude extract. Isolation of O-acetylserine sulfhydrylases A and B and beta-cystathionase based on their ability to mobilize sulfur from cysteine and to participate in Fe-S cluster synthesis. J. Biol. Chem. 271:16053-16067.
11. Gehrke, C. W., K. C. Kuo, R. A. McCune, and K. Gerhardt. 1982. Quantitative enzymatic hydrolysis of tRNAs. Reversed-phase high-perfirmance liquid chromatography of tRNA nucleosides. J. Chromatogr. 230:297-308.
12. Griffiths, E., J. Humphreys, A. Leach, and L. Scanlon. 1978. Alterations in the tRNAs of Escherichia coli recovered from lethally infected animals. Infect. Immun. 22:312-317.
13. Hamilton, C. M., M. Aldea, B. K. Washburn, P. Babitzke, and S. R. Kushner. 1989. New method for generating deletions and gene replacements in Escherichia coli. J. Bacteriol. 171:4617-4622.
14. Kambampati, R., and C. T. Lauhon. 2000. IscS is a sulfurtransferase for the in vitro biosynthesis of 4-thiouridine in Escherichia coli tRNA. Biochemistry 38:16561-16568.
15. 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.
16. Kramer, G. F., J. C. Baker, and B. N. Ames. 1988. Near-UV stress in Salmonella typhimurium: 4-thiouridine in tRNA, ppGpp, and ApppGpp as components of an adaptive response. J. Bacteriol. 170:2344-2351.
17. 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. 275:20096-21003.
18. Leimkuhler, S., and K. V. Rajagopalan. 2001. A sulfurtransferase is required in the transfer of cysteine sulfur in the in vitro synthesis of molybdopterin from precursor Z in Escherichia coli. J. Biol. Chem. 276:22024-22031.
19. Li, J., M. Kogan, S. A. B. Knight, D. Pain, and A. Dancis. 1999. Yeast mitochondrial protein, Nfs1p, coordinately regulates iron-sulfur cluster proteins, cellular iron uptake, and iron distribution. J. Biol. Chem. 274:33025-33034.
20. 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.
21. 2 modifications of U34. Eur. J. Biochem. 266:1128-1135.
22. Marquet, A. 2001. Enzymology of carbon-sulfur bond formation. Curr. Opin. Chem. Biol. 5:541-549.
23. Mihara, H., S. Kato, G. M. Lacourciere, T. C. Stadtman, R. A. Kennedy, T. Kurihara, U. Tokumoto, Y. Takahashi, and N. Esaki. 2002. The iscS gene is essential for the biosynthesis of 2-selenouridine in tRNA and the selenocysteine-containing formate dehydrogenase H. Proc. Natl. Acad. Sci. USA 99:6679-6683.
24. Mihara, H., T. Kurihara, T. Yoshimura, K. Soda, and N. Esaki. 1997. Cysteine sulfinate desulfinase, an NIFS-like protein of Escherichia coli with selenocysteine lyase and cysteine desulfurase activities. Gene cloning, purification, and characterization of a novel pyridoxal enzyme. J. Biol. Chem. 272:22417-22424.
25. Mihara, H., M. Maeda, T. Fujii, T. Kurihara, Y. Hata, and N. Esaki. 1999. A nifS-like gene, csdB, encodes an Escherichia coli counterpart of mammalian selenocysteine lyase. Gene cloning, purification, characterization, and preliminary x-ray crystallographic studies. J. Biol. Chem. 274:14768-14772.
26. Mihara, H., T. Kurihara, T. Yoshimura, and N. Esaki. 2000. Kinetic and mutational studies of three NifS homologs from Escherichia coli: mechanistic difference between L-cysteine desulfurase and L-selenocysteine lyase reactions. J. Biochem. (Tokyo) 127:559-567.
27. Mueller, E. G., C. J. Buck, P. M. Palenchar, L. E. Barnhart, and J. L. Paulson. 1998. Identification of a gene involved in the generation of 4-thiouridine in tRNA. Nucleic Acids Res. 26:2606-2610.
28. 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.
29. Patzer, S. I., and K. Hantke. 1999. SufS is a NifS-like protein, and SufD is necessary for stability of the [2Fe-2S] FhuF protein in Escherichia coli. J. Bacteriol. 181:3307-3309.
30. Pierrel, F., G. R. Bjork, M. Fontecave, and M. Atta. 2002. Enzymatic modification of tRNAs: MiaB is an iron-sulfur protein. J. Biol. Chem. 277:13367-13370.
31. Ryals, J., R.-Y. Hsu, M. N. Lipsett, and H. Bremer. 1982. Isolation of single-Site Escherichia coli mutants deficient in thiamine and 4-thiouridine syntheses: identification of a nuvC mutant. J. Bacteriol. 151:899-904.
32. Schwartz, C. J., O. Djaman, J. A. Imlay, and P. J. Kiley. 2000. The cysteine desulfurase IscS has a major role in in vivo Fe-S cluster formation in Escherichia coli. J. Bacteriol. 97:9009-9014.
33. 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.
34. 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.
35. Sofia, H. J., G. Chen, B. G. Hetzler, J. F. Reyes-Spindola, and N. E. Miller. 2001. Radical SAM, a novel protein superfamily linking unresolved steps in familiar biosynthetic pathways with radical mechanisms: functional characterization with new analysis and information visualization methods. Nucleic Acids Res. 29:1097-1106.
36. Sullivan, M. A., J. F. Cannon, F. H. Webb, and R. Bock. 1985. Antisuppressor mutation in Escherichia coli defective in biosynthesis of 5-methylaminomethyl-2-thiouridine. J. Bacteriol. 161:368-376.
37. Glu is a positive determinant for aminoacylation by Escherichia coli glutamyl-tRNA synthetase. Biochemistry 32:3836-3841.
38. Takahashi, Y., and U. Tokumoto. 2002. A third bacterial system for the assembly of iron-sulfur clusters with homologs in archaea and plastids. J. Biol. Chem. 277:28380-28383.
39. 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.
40. 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.
41. Urbina, H. D., J. J. Silberg, K. G. Hoff, and L. Vickery. 2001. Transfer of sulfur from IscS to IscU during Fe/S cluster assembly. J. Biol. Chem. 276:44521-44526.
42. Urbonavicius, J., Q. Qian, J. M. Durand, T. G. Hagervall, and G. R. Bjork. 2001. Improvement of reading frame maintenance is a common function for several tRNA modifications. EMBO J. 20:4863-4873.
43. Webb, E., K. Class, and D. M. Downs. 1997. Characterization of thil, a new gene involved in thiazole biosynthesis in Salmonella typhimurium. J. Bacteriol. 179:4399-4402.
44. Xi, J., Y. Ge, C. Kinsland, F. W. McLafferty, and T. P. Begley. 2001. Biosynthesis of the thiazole moiety of thiamin in Escherichia coli: identification of an acyldisulfide-linked protein-protein conjugate that is functionally analogous to the ubiquitin/E1 complex. Proc. Natl. Acad. Sci. USA 98:8513-8518.
45. 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.
46. Zheng, L., V. L. Cash, D. H. Flint, and D. R. Dean. 1998. Assembly of iron-sulfur clusters. Identification of an iscSUA-hscBA-fdx gene cluster from Azotobacter vinelandii. J. Biol. Chem. 273:13264-13272.
47. Zheng, L., R. H. White, V. L. Cash, R. F. Jack, and D. R. Dean. 1993. Cysteine desulfurase activity indicates a role for NIFS in metallocluster biosynthesis. Proc. Nat. Acad. Sci. USA 90:2754-2758.