The tRNA thiolation pathway modulates the intracellular redox state in Escherichia coli

Journal of Bacteriology

Volumn 195, Issue 9, 2013, Pages 2039-2049

  Nakayashiki, Toru ^a   Saito, Natsumi ^b   Takeuchi, Rikiya ^a   Kadokura, Hiroshi ^a   Nakahigashi, Kenji ^b   Wanner, Barry L ^c   Mori, Hirotada ^a,b  

^a NARA INSTITUTE OF SCIENCE AND TECHNOLOGY   (Japan)

^b KEIO UNIVERSITY   (Japan)

^c PURDUE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

5 METHYLAMINOMETHYL 2 THIOURIDINE; ADENOSINE DIPHOSPHATE; ADENOSINE TRIPHOSPHATE; DEOXYNUCLEOSIDE TRIPHOSPHATE; DEOXYRIBONUCLEOTIDE; HYDROXYUREA; PHOSPHOTRANSFERASE; RIBONUCLEOTIDE REDUCTASE; THIOURIDINE; TRANSFER RNA; UNCLASSIFIED DRUG;

ARTICLE; CATALYSIS; CELL RESPIRATION; DISULFIDE BOND; ESCHERICHIA COLI; GENE DELETION; MOLECULAR BIOLOGY; MUTANT; NONHUMAN; OXIDATION REDUCTION REACTION; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN MODIFICATION; REAL TIME POLYMERASE CHAIN REACTION; SCREENING TEST; THIOLATION;

ADENOSINE DIPHOSPHATE; ADENOSINE TRIPHOSPHATE; ESCHERICHIA COLI K12; ESCHERICHIA COLI PROTEINS; HYDROXYUREA; MUTATION; OXIDATION-REDUCTION; RIBONUCLEOTIDE REDUCTASES; RNA, TRANSFER; THIOURIDINE;

ESCHERICHIA COLI; ESCHERICHIA COLI K12;

EID: 84876176054     PISSN: 00219193     EISSN: 10985530     Source Type: Journal    
DOI: 10.1128/JB.02180-12     Document Type: Article

References (44)

1. Baba T, Ara T, Hasegawa M, Takai Y, Okumura Y, Baba M, Datsenko KA, Tomita M, Wanner BL, Mori H. 2006. Construction of Escherichia coli K-12 in-frame, single-gene knockout mutants: the Keio Collection. Mol. Syst. Biol. 2:2006-0008. doi:10.1038/msb4100050.
2. Odsbu I, Morigen Skarstad K. 2009. A reduction in ribonucleotide reductase activity slows down the chromosome replication fork but does not change its localization. PLoS One 4:e7617. doi:10.1371/journal.pone .0007617.
3. Davies BW, Kohanski MA, Simmons LA, Winkler JA, Collins JJ, Walker GC. 2009. Hydroxyurea induces hydroxyl radical-mediated cell death in Escherichia coli. Mol. Cell 36:845-860.
4. Nordlund P, Reichard P. 2006. Ribonucleotide reductases. Annu. Rev. Biochem. 75:681-706.
5. Eklund H, Uhlin U, Färnegårdh M, Logan DT, Nordlund P. 2001. Structure and function of the radical enzyme ribonucleotide reductase. Prog. Biophys. Mol. Biol. 77:177-268.
6. Jordan A, Aragall E, Gibert I, Barbe J. 1996. Promoter identification and expression analysis of Salmonella typhimurium and Escherichia coli nrdEF operons encoding one of two class I ribonucleotide reductases present in both bacteria. Mol. Microbiol. 19:777-790.
7. Gibert I, Calero S, Barbé J. 1990. Measurement of in vivo expression of nrdA and nrdB genes of Escherichia coli by using lacZ gene fusions. Mol. Gen. Genet. 220:400-408.
8. Herrick J, Sclavi B. 2007. Ribonucleotide reductase and the regulation of DNA replication: an old story and an ancient heritage. Mol. Microbiol. 63:22-34.
9. Olliver A, Saggioro C, Herrick J, Sclavi B. 2010. DnaA-ATP acts as a molecular switch to control levels of ribonucleotide reductase expression in Escherichia coli. Mol. Microbiol. 76:1555-1571.
10. Sitjes J, Ysern P, Barbe J, Llagostera M. 1992. Induction of ribonucleoside diphosphate reductase gene transcription by chemicals in Escherichia coli. Mutagenesis 7:47-49.
11. Grinberg I, Shteinberg T, Hassan AQ, Aharonowitz Y, Borovok I, Cohen G. 2009. Functional analysis of the Streptomyces coelicolor NrdR ATP-cone domain: role in nucleotide binding, oligomerization, and DNA interactions. J. Bacteriol. 191:1169-1179.
12. Augustin LB, Jacobson BA, Fuchs JA. 1994. Escherichia coli Fis and DnaA proteins bind specifically to the nrd promoter region and affect expression of an nrd-lac fusion. J. Bacteriol. 176:378-387.
13. Gon S, Camara JE, KlungsØyr HK, Crooke E, Skarstad K, Beckwith J. 2006.Anovel regulatory mechanism couples deoxyribonucleotide synthesis and DNA replication in Escherichia coli. EMBO J. 25:1137-1147.
14. Datsenko KA, Wanner BL. 2000. One-step inactivation of chromosomal genes in Escherichia coli K-12 using PCR products. Proc. Natl. Acad. Sci. U. S. A. 97:6640-6645.
15. Cherepanov PP, Wackernagel W. 1995. Gene disruption in Escherichia coli: TcR and KmR cassettes with the option of Flp-catalyzed excision of the antibiotic-resistance determinant. Gene 158:9-14.
16. Takeshita S, Sato M, Toba M, Masahashi W, Hashimoto-Gotoh T. 1987. High-copy-number and low-copy-number plasmid vectors for lacZ alpha-complementation and chloramphenicol- or kanamycin-resistance selection. Gene 61:63-74.
17. Kitagawa M, Ara T, Arifuzzaman M, Ioka-Nakamichi T, Inamoto E, Toyonaga H, Mori H. 2005. Complete set of ORF clones of Escherichia coli ASKA library (a complete set of E. coli K-12 ORF archive): unique resources for biological research. DNA Res. 12:291-299.
18. Lawless C, Wilkinson DJ, Young A, Addinall SG, Lydall DA, Lu M, Campbell JL. 2010. Colonyzer: automated quantification of microorganism growth characteristics on solid agar. BMC Bioinformatics 11: 287. doi:10.1186/1471-2105-11-287.
19. Saito N, Robert M, Kochi H, Matsuo G, Kakazu Y, Soga T, Tomita M. 2009. Metabolite profiling reveals YihU as a novel hydroxybutyrate dehydrogenase for alternative succinic semialdehyde metabolism in Escherichia coli. J. Biol. Chem. 284:16442-16451.
20. Ikeuchi Y, Shigi N, Kato J, Nishimura A, Suzuki T. 2006. Mechanistic insights into sulfur relay by multiple sulfur mediators involved in thiouridine biosynthesis at tRNA wobble positions. Mol. Cell 21:97-108.
21. McCool JD, Long E, Petrosino JF, Sandler HA, Rosenberg SM, Sandler SJ. 2004. Measurement of SOS expression in individual Escherichia coli K-12 cells using fluorescence microscopy. Mol. Microbiol. 53:1343-1357.
22. Messner KR, Imlay JA. 2002. In vitro quantitation of biological superoxide and hydrogen peroxide generation. Methods Enzymol. 349:354-361.
23. Barbé J, Villaverde A, Guerrero R. 1987. Induction of the SOS response by hydroxyurea in Escherichia coli K12. Mutat. Res. 192:105-108. 24. Stubbe J. 2003. Di-iron-tyrosyl radical ribonucleotide reductases. Curr. Opin. Chem. Biol. 7:183-188.
24. Stubbe J. 2003. Di-iron-tyrosyl radical ribonucleotide reductases. Curr. Opin. Chem. Biol. 7:183-188.
25. Torrents E, Grinberg I, Gorovitz-Harris B, Lundström H, Borovok I, Aharonowitz Y, Sjöberg BM, Cohen G. 2007. NrdR controls differential expression of the Escherichia coli ribonucleotide reductase genes. J. Bacteriol. 189:5012-5021.
26. Grinberg I, Shteinberg T, Gorovitz B, Aharonowitz Y, Cohen G, Borovok I. 2006. The Streptomyces NrdR transcriptional regulator is a Zn ribbon/ATP cone protein that binds to the promoter regions of class Ia and class II ribonucleotide reductase operons. J. Bacteriol. 188:7635-7644.
27. Schulze KL, Lipe RS. 1964. Relationship between substrate concentration, growth rate, and respiration rate of Escherichia coli in continuous culture. Arch. Mikrobiol. 48:1-20.
28. Andersen KB, von Meyenburg K. 1980. Are growth rates of Escherichia coli in batch cultures limited by respiration? J. Bacteriol. 144:114-123.
29. Kessler D. 2006. Enzymatic activation of sulfur for incorporation into biomolecules in prokaryotes. FEMS Microbiol. Rev. 30:825-840.
30. Mueller EG. 2006. Trafficking in persulfides: delivering sulfur in biosynthetic pathways. Nat. Chem. Biol. 2:185-194.
31. Francoleon NE, Carrington SJ, Fukuto JM. 2011. The reaction of H2S with oxidized thiols: generation of persulfides and implications to H2S biology. Arch. Biochem. Biophys. 516:146-153.
32. Imlay JA. 2008. Cellular defenses against superoxide and hydrogen peroxide. Annu. Rev. Biochem. 77:755-776.
33. Zheng M, Aslund F, Storz G. 1998. Activation of the OxyR transcription factor by reversible disulfide bond formation. Science 279:1718-1721.
34. 2S signals through protein Ssulfhydration. Sci. Signal. 2:ra72. doi:10.1126/scisignal.2000464.
35. Åslund F, Ehn B, Miranda-Vizuete A, Pueyo C, Holmgren A. 1994. Two additional glutaredoxins exist in Escherichia coli: glutaredoxin 3 is a hydrogen donor for ribonucleotide reductase in a thioredoxin/glutaredoxin 1 double mutant. Proc. Natl. Acad. Sci. U. S. A. 91:9813-9817.
36. Seaver LC, Imlay JA. 2001. Alkyl hydroperoxide reductase is the primary scavenger of endogenous hydrogen peroxide in Escherichia coli. J. Bacteriol. 183:7173-7181.
37. Poole LB. 2005. Bacterial defenses against oxidants: mechanistic features of cysteine-based peroxidases and their flavoprotein reductases. Arch. Biochem. Biophys. 433:240-254.
38. Dahl C, Engels S, Pott-Sperling AS, Schulte A, Sander J, Lübbe Y, Deuster O, Brune DC. 2005. 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. 187:1392-1404.
39. Pott AS, Dahl C. 1998. Sirohaem sulfite reductase and other proteins encoded by genes at the dsr locus of Chromatium vinosum are involved in the oxidation of intracellular sulfur. Microbiology 144:1881-1894.
40. Rubinstein ND, Zeevi D, Oren Y, Segal G, Pupko T. 2011. The operonic location of auto-transcriptional repressors is highly conserved in bacteria. Mol. Biol. Evol. 28:3309-3318.
41. Hefti MH, Françoijs KJ, de Vries SC, Dixon R, Vervoort J. 2004. The PAS fold. A redefinition of the PAS domain based upon structural prediction. Eur. J. Biochem. 271:1198-1208.
42. Ahluwalia D, Bienstock RJ, Schaaper RM. 2012. Novel mutator mutants of E. coli nrdAB ribonucleotide reductase: insight into allosteric regulation and control of mutation rates. DNA Repair 11:480-487.
43. Ortenberg R, Gon S, Porat A, Beckwith J. 2004. Interactions of glutaredoxins, ribonucleotide reductase, and components of the DNA replication system of. Escherichia coli. Proc. Natl. Acad. Sci. U. S. A. 101:7439-7444.
44. Watanabe K, Hayashi N, Oyama A, Nishikawa K, Ueda T, Miura K. 1994. Unusual anticodon loop structure found in E. coli lysine tRNA. Nucleic Acids Res. 22:79-87.