Mechanistic insights into sulfur relay by multiple sulfur mediators involved in thiouridine biosynthesis at tRNA wobble positions

Molecular Cell

Volumn 21, Issue 1, 2006, Pages 97-108

  Ikeuchi, Yoshiho ^a   Shigi, Naoki ^b   Kato, Jun Ichi ^c   Nishimura, Akiko ^d,e   Suzuki, Tsutomu ^a  

^a UNIVERSITY OF TOKYO   (Japan)

^b NATIONAL INSTITUTE OF ADVANCED INDUSTRIAL SCIENCE AND TECHNOLOGY AIST   (Japan)

^c TOKYO METROPOLITAN UNIVERSITY   (Japan)

^d NATIONAL INSTITUTE OF GENETICS   (Japan)

^e Yoshida Biological Laboratory Inc   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

5 METHYLAMINOMETHYL 2 THIOURIDINE; BACTERIAL PROTEIN; BACTERIAL RNA; PROTEIN ISCS; PROTEIN MNMA; PROTEIN TUSA; PROTEIN TUSBCD COMPLEX; PROTEIN TUSD; PROTEIN TUSE; RECOMBINANT PROTEIN; SULFIDE; SULFUR; THIOURIDINE; TRANSFER RNA; UNCLASSIFIED DRUG;

ACCURACY; ARTICLE; BACTERIAL GENE; BIOSYNTHESIS; CELL GROWTH; CODON; CONTROLLED STUDY; ENZYME ACTIVATION; ENZYME ACTIVITY; ENZYME SUBSTRATE COMPLEX; GENE IDENTIFICATION; GENETIC CODE; GENETIC SCREENING; GENOME ANALYSIS; IN VITRO STUDY; MEDIATOR; NONHUMAN; PROTEIN MODIFICATION; PROTEIN PROTEIN INTERACTION; PROTEIN RNA BINDING; PYRIMIDINE SYNTHESIS; REGULATORY MECHANISM;

AMINO ACID SEQUENCE; CARBON-SULFUR LYASES; ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; MACROMOLECULAR SUBSTANCES; MOLECULAR SEQUENCE DATA; NUCLEIC ACID CONFORMATION; RECOMBINANT PROTEINS; RNA PROCESSING, POST-TRANSCRIPTIONAL; RNA, BACTERIAL; RNA, TRANSFER; SEQUENCE ALIGNMENT; SULFUR; THIOURIDINE;

BACTERIA (MICROORGANISMS);

EID: 29544452864     PISSN: 10972765     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.molcel.2005.11.001     Document Type: Article

References (47)

1. P.F. Agris, D. Soll, and T. Seno Biological function of 2-thiouridine in Escherichia coli glutamic acid transfer ribonucleic acid Biochemistry 12 1973 4331 4337
2. A. Alexandrov, M.R. Martzen, and E.M. Phizicky Two proteins that form a complex are required for 7-methylguanosine modification of yeast tRNA RNA 8 2002 1253 1266
3. S.S. Ashraf, E. Sochacka, R. Cain, R. Guenther, A. Malkiewicz, and P.F. Agris Single atom modification (O→S) of tRNA confers ribosome binding RNA 5 1999 188 194
4. A.G. Atherly Escherichia coli mutant containing a large deletion from relA to argA J. Bacteriol. 138 1979 530 534
5. F.R. Blattner, G. Plunkett 3rd, C.A. Bloch, N.T. Perna, V. Burland, M. Riley, J. Collado-Vides, J.D. Glasner, C.K. Rode, and G.F. Mayhewet The complete genome sequence of Escherichia coli K-12 Science 277 1997 1453 1474
6. P. Bork, and E.V. Koonin A P-loop-like motif in a widespread ATP pyrophosphatase domain: implications for the evolution of sequence motifs and enzyme activity Proteins 20 1994 347 355
7. J.R. Cort, S.V. Mariappan, C.Y. Kim, M.S. Park, T.S. Peat, G.S. Waldo, T.C. Terwilliger, and M.A. Kennedy Solution structure of Pyrobaculum aerophilum DsrC, an archaeal homologue of the gamma subunit of dissimilatory sulfite reductase Eur. J. Biochem. 268 2001 5842 5850
8. Crain, P.F., Rozenski, J., and McCloskey, J.A. (1999). The RNA modification database (http://medstat.med.utah.edu/RNAmods/).
9. J.R. Cupp-Vickery, H. Urbina, and L.E. Vickery Crystal structure of IscS, a cysteine desulfurase from Escherichia coli J. Mol. Biol. 330 2003 1049 1059
10. J.F. Curran Modified nucleosides in translation H. Grosjean R. Benne Modification and Editing of RNA 1998 ASM Press Washington, D.C. 463 516
11. C. Dahl, S. Engels, A.S. Pott-Sperling, A. Schulte, J. Sander, Y. Lubbe, O. Deuster, and D.C. Brune Novel genes of the dsr gene cluster and evidence for close interaction of Dsr proteins during sulfur oxidation in the phototrophic sulfur bacterium Allochromatium vinosum J. Bacteriol. 187 2005 1392 1404
12. L.G. De Bie, M. Roovers, Y. Oudjama, R. Wattiez, C. Tricot, V. Stalon, L. Droogmans, and J.M. Bujnicki The yggH gene of Escherichia coli encodes a tRNA (m7G46) methyltransferase J. Bacteriol. 185 2003 3238 3243
13. A.L. Fimmel, and R.E. Loughlin Isolation of a lambdadcys transducing bacteriophage and its use in determining the regulation of cysteine messenger ribonucleic acid synthesis in Escherichia coli K-12 J. Bacteriol. 132 1977 757 763
14. J. Frazzon, and D.R. Dean Formation of iron-sulfur clusters in bacteria: an emerging field in bioinorganic chemistry Curr. Opin. Chem. Biol. 7 2003 166 173
15. J.D. Glasner, P. Liss, G. Plunkett 3rd, A. Darling, T. Prasad, M. Rusch, A. Byrnes, M. Gilson, B. Biehl, F.R. Blattner, and N.T. Perna ASAP, a systematic annotation package for community analysis of genomes Nucleic Acids Res. 31 2003 147 151
16. Y. Ikeuchi, A. Soma, T. Ote, J. Kato, Y. Sekine, and T. Suzuki Molecular mechamism of lysidine synthesis that determines tRNA identity and codon recognition Mol. Cell 19 2005 235 246
17. R. Kambampati, and C.T. Lauhon IscS is a sulfurtransferase for the in vitro biosynthesis of 4-thiouridine in Escherichia coli tRNA Biochemistry 38 1999 16561 16568
18. R. Kambampati, and C.T. Lauhon MnmA and IscS are required for in vitro 2-thiouridine biosynthesis in Escherichia coli Biochemistry 42 2003 1109 1117
19. T. Kaneko, T. Suzuki, S.T. Kapushoc, M.A. Rubio, J. Ghazvini, K. Watanabe, L. Simpson, and T. Suzuki Wobble modification differences and subcellular localization of tRNAs in Leishmania tarentolae: implication for tRNA sorting mechanism EMBO J. 22 2003 657 667
20. S. Kato, H. Mihara, T. Kurihara, Y. Takahashi, U. Tokumoto, T. Yoshimura, and N. Esaki 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 2002 5948 5952
21. C.T. Lauhon Requirement for IscS in biosynthesis of all thionucleosides in Escherichia coli J. Bacteriol. 184 2002 6820 6829
22. C.T. Lauhon, and R. Kambampati The iscS gene in Escherichia coli is required for the biosynthesis of 4-thiouridine, thiamin, and NAD J. Biol. Chem. 275 2000 20096 20103
23. L. Loiseau, S. Ollagnier-de Choudens, D. Lascoux, E. Forest, M. Fontecave, and F. Barras Analysis of the heteromeric CsdA-CsdE cysteine desulfurase, assisting Fe-S cluster biogenesis in Escherichia coli J. Biol. Chem. 280 2005 26760 26769
24. H. Mihara, and N. Esaki Bacterial cysteine desulfurases: their function and mechanisms Appl. Microbiol. Biotechnol. 60 2002 12 23
25. Y. Nakai, N. Umeda, T. Suzuki, M. Nakai, H. Hayashi, K. Watanabe, and H. Kagamiyama Yeast Nfs1p is involved in thio-modification of both mitochondrial and cytoplasmic tRNAs J. Biol. Chem. 279 2004 12363 12368
26. K. Nakanishi, S. Fukai, Y. Ikeuchi, A. Soma, Y. Sekine, T. Suzuki, and O. Nureki Structural basis for lysidine formation by ATP pyrophosphatase accompanied by a lysine-specific loop and a tRNA-recognition domain Proc. Natl. Acad. Sci. USA 102 2005 7487 7492
27. K. Nilsson, H.K. Lundgren, T.G. Hagervall, and G.R. Bjork The cysteine desulfurase IscS is required for synthesis of all five thiolated nucleosides present in tRNA from Salmonella enterica serovar typhimurium J. Bacteriol. 184 2002 6830 6835
28. H. Okamoto, K. Watanabe, Y. Ikeuchi, T. Suzuki, Y. Endo, and H. Hori Substrate tRNA recognition mechanism of tRNA (m7G46) methyltransferase from Aquifex aeolicus J. Biol. Chem. 279 2004 49151 49159
29. S. Ollagnier-de-Choudens, D. Lascoux, L. Loiseau, F. Barras, E. Forest, and M. Fontecave Mechanistic studies of the SufS-SufE cysteine desulfurase: evidence for sulfur transfer from SufS to SufE FEBS Lett. 555 2003 263 267
30. P.M. Palenchar, C.J. Buck, H. Cheng, T.J. Larson, and E.G. Mueller Evidence that ThiI, an enzyme shared between thiamin and 4-thiouridine biosynthesis, may be a sulfurtransferase that proceeds through a persulfide intermediate J. Biol. Chem. 275 2000 8283 8286
31. A.S. Pott, and C. Dahl Sirohaem sulfite reductase and other proteins encoded by genes at the dsr locus of Chromatium vinosum are involved in the oxidation of intracellular sulfur Microbiol. 144 1998 1881 1894
32. J.S. Reader, D. Metzgar, P. Schimmel, and V. de Crecy-Lagard Identification of four genes necessary for biosynthesis of the modified nucleoside queuosine J. Biol. Chem. 279 2004 6280 6285
33. J. Rozenski, P.F. Crain, and J.A. McCloskey The RNA Modification Database: 1999 update Nucleic Acids Res. 27 1999 196 197
34. K. Saka, M. Tadenuma, S. Nakade, N. Tanaka, H. Sugawara, K. Nishikawa, N. Ichiyoshi, M. Kitagawa, H. Mori, N. Ogasawara, and A. Nishimura A complete set of Escherichia coli open reading frames in mobile plasmids facilitating genetic studies DNA Res. 12 2005 63 68
35. C.J. Schwartz, O. Djaman, J.A. Imlay, and P.J. Kiley The cysteine desulfurase, IscS, has a major role in in vivo Fe-S cluster formation in Escherichia coli Proc. Natl. Acad. Sci. USA 97 2000 9009 9014
36. A. Soma, Y. Ikeuchi, S. Kanemasa, K. Kobayashi, N. Ogasawara, T. Ote, J. Kato, K. Watanabe, Y. Sekine, and T. Suzuki An RNA-modifying enzyme that governs both the codon and amino acid specificities of isoleucine tRNA Mol. Cell 12 2003 689 698
37. T. Suzuki Biosynthesis and function of tRNA wobble modifications H. Grosjean Topics in Current Genetics 2005 Springer-Verlag New York 24 69
38. L.A. Sylvers, K.C. Rogers, M. Shimizu, E. Ohtsuka, and D. Soll A 2-thiouridine derivative in tRNAGlu is a positive determinant for aminoacylation by Escherichia coli glutamyl-tRNA synthetase Biochemistry 32 1993 3836 3841
39. H. Tabor, C.W. Tabor, M.S. Cohn, and E.W. Hafner Streptomycin resistance (rpsL) produces an absolute requirement for polyamines for growth of an Escherichia coli strain unable to synthesize putrescine and spermidine J. Bacteriol. 147 1981 702 704
40. S.V. Taylor, N.L. Kelleher, C. Kinsland, H.J. Chiu, C.A. Costello, A.D. Backstrom, F.W. McLafferty, and T.P. Begley Thiamin biosynthesis in Escherichia coli. Identification of this thiocarboxylate as the immediate sulfur donor in the thiazole formation J. Biol. Chem. 273 1998 16555 16560
41. N. Umeda, T. Suzuki, M. Yukawa, Y. Ohya, H. Shindo, K. Watanabe, and T. Suzuki Mitochondria-specific RNA-modifying enzymes responsible for the biosynthesis of the wobble base in mitochondrial tRNAs. Implications for the molecular pathogenesis of human mitochondrial diseases J. Biol. Chem. 280 2005 1613 1624
42. H.D. Urbina, J.J. Silberg, K.G. Hoff, and L.E. Vickery Transfer of sulfur from IscS to IscU during Fe/S cluster assembly J. Biol. Chem. 276 2001 44521 44526
43. C.M. Wright, P.M. Palenchar, and E.G. Mueller A paradigm for biological sulfur transfers via persulfide groups: a persulfide-disulfide-thiol cycle in 4-thiouridine biosynthesis Chem. Commun. (Camb.) 2002 2708 2709
44. T. Yamashino, M. Isomura, C. Ueguchi, and T. Mizuno The yhhP gene encoding a small ubiquitous protein is fundamental for normal cell growth of Escherichia coli J. Bacteriol. 180 1998 2257 2261
45. C. Yarian, M. Marszalek, E. Sochacka, A. Malkiewicz, R. Guenther, A. Miskiewicz, and P.F. Agris Modified nucleoside dependent Watson-Crick and wobble codon binding by tRNALysUUU species Biochemistry 39 2000 13390 13395
46. S. Yokoyama, and S. Nishimura Modified nucleosides and codon recognition D. Soll U.L. RajBhandary tRNA: Structure, Biosynthesis, and Function 1995 American Society for Microbiology Washington, D.C. 207 224
47. S. Yokoyama, T. Watanabe, K. Murao, H. Ishikura, Z. Yamaizumi, S. Nishimura, and T. Miyazawa Molecular mechanism of codon recognition by tRNA species with modified uridine in the first position of the anticodon Proc. Natl. Acad. Sci. USA 82 1985 4905 4909