IscR-dependent gene expression links iron-sulphur cluster assembly to the control of O2-regulated genes in Escherichia coli

Molecular Microbiology

Volumn 60, Issue 4, 2006, Pages 1058-1075

  Giel, Jennifer L ^a   Rodionov, Dmitry ^b,c   Liu, Mingzhu ^a   Blattner, Frederick R ^a   Kiley, Patricia J ^a  

^a UNIVERSITY OF WISCONSIN MADISON   (United States)

^b INSTITUTE FOR INFORMATION TRANSMISSION PROBLEMS   (Russian Federation)

^c BURNHAM INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DEOXYRIBONUCLEASE I; HYAABCDEF PROTEIN; HYBABCDEFG PROTEIN; IRON SULFUR PROTEIN; NAPFDAGHBC PROTEIN; OXYGEN; PROTEIN; SUFABCDSE PROTEIN; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR ISCR; UNCLASSIFIED DRUG; YADR PROTEIN; YHGI PROTEIN;

AEROBIC METABOLISM; ANAEROBIC METABOLISM; ARTICLE; BACTERIAL GENE; BACTERIAL STRAIN; BINDING SITE; ESCHERICHIA COLI; FDX GENE; GENE CONTROL; GENE EXPRESSION; GENE EXPRESSION REGULATION; GENE REPRESSION; GENETIC TRANSCRIPTION; HSCBA GENE; HYA GENE; HYO GENE; ISCSUA GENE; NAPF GENE; NONHUMAN; OPERON; PHYLOGENY; PRIORITY JOURNAL; PROTEIN ASSEMBLY; TRANSCRIPTION PROFILING;

ANAEROBIOSIS; BASE SEQUENCE; ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, BACTERIAL; GENES, BACTERIAL; IRON-SULFUR PROTEINS; MOLECULAR SEQUENCE DATA; MULTIGENE FAMILY; OXIDATIVE STRESS; OXYGEN; PROMOTER REGIONS (GENETICS); SUPEROXIDE DISMUTASE; TRANSCRIPTION FACTORS;

BACTERIA (MICROORGANISMS); ESCHERICHIA COLI; HYA;

EID: 33646427470     PISSN: 0950382X     EISSN: 13652958     Source Type: Journal    
DOI: 10.1111/j.1365-2958.2006.05160.x     Document Type: Article

References (63)

1. Agar JN Krebs C Frazzon J Huynh BH Dean DR Johnson MK 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. Benson DA Karsch-Mizrachi I Lipman DJ Ostell J Wheeler DL 2005 GenBank Nucleic Acids Res 33 1
3. Bockhorst J Qiu Y Glasner J Liu M Blattner F Craven M 2003 Predicting bacterial transcription units using sequence and expression data Bioinformatics 19 Suppl. i34 43
4. Brondsted L Atlung T 1994 Anaerobic regulation of the hydrogenase 1 (hya) operon of Escherichia coli J Bacteriol 176 5423 5428
5. Butland G Peregrin-Alvarez JM Li J Yang W Yang X Canadien V et al. 2005 Interaction network containing conserved and essential protein complexes in Escherichia coli Nature 433 531 537
6. Chenna R Sugawara H Koike T Lopez R Gibson TJ Higgins DG Thompson JD 2003 Multiple sequence alignment with the Clustal series of programs Nucleic Acids Res 31 3497 3500
7. Choe M Reznikoff WS 1991 Anaerobically expressed Escherichia coli genes identified by operon fusion techniques J Bacteriol 173 6139 6146
8. Choe M Reznikoff WS 1993 Identification of the regulatory sequence of anaerobically expressed locus aeg-46.5 J Bacteriol 175 1165 1172
9. Compan I Touati D 1993 Interaction of six global transcription regulators in expression of manganese superoxide dismutase in Escherichia coli K-12 J Bacteriol 175 1687 1696
10. Crooks GE Hon G Chandonia JM Brenner SE 2004 WebLogo: a sequence logo generator Genome Res 14 1188 1190
11. Darwin AJ Stewart V 1995 Nitrate and nitrite regulation of the Fnr-dependent aeg-46.5 promoter of Escherichia coli K-12 is mediated by competition between homologous response regulators (NarL and NarP) for a common DNA-binding site J Mol Biol 251 15 29
12. Darwin AJ Ziegelhoffer EC Kiley PJ Stewart V 1998 Fnr, NarP, and NarL regulation of Escherichia coli K-12 napF (periplasmic nitrate reductase) operon transcription in vitro J Bacteriol 180 4192 4198
13. Datsenko KA Wanner BL 2000 One-step inactivation of chromosomal genes in Escherichia coli K-12 using PCR products Proc Natl Acad Sci USA 97 6640 6645
14. Ding H Clark RJ 2004 Characterization of iron binding in IscA, an ancient iron-sulphur cluster assembly protein Biochem J 379 433 440
15. Dombrecht B Tesfay MZ Verreth C Heusdens C Napoles MC Vanderleyden J Michiels J 2002 The Rhizobium etli gene iscN is highly expressed in bacteroids and required for nitrogen fixation Mol Genet Genomics 267 820 828
16. Enz S Braun V Crosa JH 1995 Transcription of the region encoding the ferric dicitrate-transport system in Escherichia coli: similarity between promoters for fecA and for extracytoplasmic function sigma factors Gene 163 13 18
17. Flint DH 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
18. Florea L McClelland M Riemer C Schwartz S Miller W 2003 EnteriX 2003: visualization tools for genome alignments of Enterobacteriaceae Nucleic Acids Res 31 3527 3532
19. Gelfand MS Koonin EV Mironov AA 2000 Prediction of transcription regulatory sites in Archaea by a comparative genomic approach Nucleic Acids Res 28 695 705
20. Goldsmith-Fischman S Kuzin A Edstrom WC Benach J Shastry R Xiao R et al. 2004 The SufE sulfur-acceptor protein contains a conserved core structure that mediates interdomain interactions in a variety of redox protein complexes J Mol Biol 344 549 565
21. Gyaneshwar P Paliy O McAuliffe J Popham DL Jordan MI Kustu S 2005 Sulfur and nitrogen limitation in Escherichia coli K-12: specific homeostatic responses J Bacteriol 187 1074 1090
22. Hama H Kayahara T Ogawa W Tsuda M Tsuchiya T 1994 Enhancement of serine-sensitivity by a gene encoding rhodanese-like protein in Escherichia coli J Biochem (Tokyo) 115 1135 1140
23. Hidalgo E Demple B 1994 An iron-sulfur center essential for transcriptional activation by the redox-sensing SoxR protein EMBO J 13 138 146
24. Hoff KG Silberg JJ Vickery LE 2000 Interaction of the iron-sulfur cluster assembly protein IscU with the Hsc66/Hsc20 molecular chaperone system of Escherichia coli Proc Natl Acad Sci USA 97 7790 7795
25. Hoff KG Ta DT Tapley TL Silberg JJ Vickery LE 2002 Hsc66 substrate specificity is directed toward a discrete region of the iron-sulfur cluster template protein IscU J Biol Chem 277 27353 27359
26. Hogg RW Voelker C Von Carlowitz I 1991 Nucleotide sequence and analysis of the mgl operon of Escherichia coli K12 Mol Gen Genet 229 453 459
27. Johnson DC Dean DR Smith AD Johnson MK 2005 Structure, function, and formation of biological Fe-S clusters Annu Rev Biochem 74 247 281
28. Kang Y Weber KD Qiu Y Kiley PJ Blattner FR 2005 Genome-wide expression analysis indicates that FNR of Escherichia coli K-12 regulates a large number of genes of unknown function J Bacteriol 187 1135 1160
29. Kiley PJ Reznikoff WS 1991 Fnr mutants that activate gene expression in the presence of oxygen J Bacteriol 173 16 22
30. Krebs C Agar JN Smith AD Frazzon J Dean DR Huynh BH Johnson MK 2001 IscA, an alternate scaffold for Fe-S cluster biosynthesis Biochemistry 40 14069 14080
31. Lee JH Yeo WS Roe JH 2003 Regulation of the sufABCDSE operon by Fur J Microbiol 41 109 114
32. Lee JH Yeo WS Roe JH 2004 Induction of the sufA operon encoding Fe-S assembly proteins by superoxide generators and hydrogen peroxide: involvement of OxyR, IHF and an unidentified oxidant-responsive factor Mol Microbiol 51 1745 1755
33. Lelivelt MJ Kawula TH 1995 Hsc66, an Hsp70 homolog in Escherichia coli, is induced by cold shock but not by heat shock J Bacteriol 177 4900 4907
34. Liu G Li Z Chiang Y Acton T Montelione GT Murray D Szyperski T 2005 High-quality homology models derived from NMR and X-ray structures of E. coli proteins YgdK and SufE suggest that all members of the YgdK/Suf E protein family are enhancers of cysteine desulfurases Protein Sci 14 1597 1608
35. Loiseau L Ollagnier-de-Choudens S Nachin L Fontecave M Barras F 2003 Biogenesis of Fe-S cluster by the bacterial Suf system: SufS and SufE form a new type of cysteine desulfurase J Biol Chem 278 38352 38359
36. Loiseau L Ollagnier-de-Choudens S Lascoux D Forest E Fontecave M Barras F 2005 Analysis of the heteromeric CsdA-CsdE cysteine desulfurase, assisting Fe-S cluster biogenesis in Escherichia coli J Biol Chem 280 26760 26769
37. McCue L Thompson W Carmack C Ryan MP Liu JS Derbyshire V Lawrence CE 2001 Phylogenetic footprinting of transcription factor binding sites in proteobacterial genomes Nucleic Acids Res 29 774 782
38. McNicholas PM Gunsalus RP 2002 The molybdate-responsive Escherichia coli ModE transcriptional regulator coordinates periplasmic nitrate reductase (napFDAGHBC) operon expression with nitrate and molybdate availability J Bacteriol 184 3253 3259
39. Martin RG Gillette WK Martin NI Rosner JL 2002 Complex formation between activator and RNA polymerase as the basis for transcriptional activation by MarA and SoxS in Escherichia coli Mol Microbiol 43 355 370
40. Maxam AM Gilbert W 1980 Sequencing end-labeled DNA with base-specific chemical cleavages Methods Enzymol 65 499 560
41. Mihara H Maeda M Fujii T Kurihara T Hata Y Esaki N 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
42. Miller JH 1972 Experiments in Molecular Genetics Plainview, NY Cold Spring Harbor Laboratory Press
43. Mironov AA Koonin EV Roytberg MA Gelfand MS 1999 Computer analysis of transcription regulatory patterns in completely sequenced bacterial genomes Nucleic Acids Res 27 2981 2989
44. Mironov AA Vinokurova NP Gel'fand MS 2000 GenomeExplorer: software for analysis of complete bacterial genomes Mol Biol 34 222 231
45. Nachin L Loiseau L Expert D Barras F 2003 SufC: an unorthodox cytoplasmic ABC/ATPase required for [Fe-S] biogenesis under oxidative stress EMBO J 22 427 437
46. Neidhardt FC Bloch PL Smith DF 1974 Culture medium for Enterobacteria J Bacteriol 119 736 747
47. Outten FW Wood MJ Munoz FM Storz G 2003 The SufE protein and the SufBCD complex enhance SufS cysteine desulfurase activity as part of a sulfur transfer pathway for Fe-S cluster assembly in Escherichia coli J Biol Chem 278 45713 45719
48. Outten FW Djaman O Storz G 2004 A suf operon requirement for Fe-S cluster assembly during iron starvation in Escherichia coli Mol Microbiol 52 861 872
49. Patzer SI Hantke K 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
50. Porco A Alonso G Isturiz T 1998 The gluconate high affinity transport of GntI in Escherichia coli involves a multicomponent complex system J Basic Microbiol 38 395 404
51. Rangachari K Davis CT Eccleston JF Hirst EM Saldanha JW Strath M Wilson RJ 2002 SufC hydrolyzes ATP and interacts with SufB from Thermotoga maritima FEBS Lett 514 225 228
52. Richard DJ Sawers G Sargent F McWalter L Boxer DH 1999 Transcriptional regulation in response to oxygen and nitrate of the operons encoding the [NiFe] hydrogenases 1 and 2 of Escherichia coli Microbiology 145 2903 2912
53. Schwartz CJ Giel JL Patschkowski T Luther C Ruzicka FJ Beinert H Kiley PJ 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
54. Seaton BL Vickery LE 1994 A gene encoding a DnaK/hsp70 homolog in Escherichia coli Proc Natl Acad Sci USA 91 2066 2070
55. Shimomura Y Takahashi Y Kakuta Y Fukuyama K 2005 Crystal structure of Escherichia coli YfhJ protein, a member of the ISC machinery involved in assembly of iron-sulfur clusters Proteins 60 566 569
56. Smith AD Agar JN Johnson KA Frazzon J Amster IJ Dean DR Johnson MK 2001 Sulfur transfer from IscS to IscU: the first step in iron-sulfur cluster biosynthesis J Am Chem Soc 123 11103 11104
57. Stewart V Bledsoe PJ Williams SB 2003 Dual overlapping promoters control napF (periplasmic nitrate reductase) operon expression in Escherichia coli K-12 J Bacteriol 185 5862 5870
58. Sutton VR Kiley PJ 2003 Techniques for studying the oxygen-sensitive transcription factor FNR from Escherichia coli Methods Enzymol 370 300 312
59. Tokumoto U Nomura S Minami Y Mihara H Kato S Kurihara T et al. 2002 Network of protein-protein interactions among iron-sulfur cluster assembly proteins in Escherichia coli J Biochem (Tokyo) 131 713 719
60. Urbina HD Silberg JJ Hoff KG Vickery LE 2001 Transfer of sulfur from IscS to IscU during Fe/S cluster assembly J Biol Chem 276 44521 44526
61. Vickery LE Silberg JJ Ta DT 1997 Hsc66 and Hsc20, a new heat shock cognate molecular chaperone system from Escherichia coli Protein Sci 6 1047 1056
62. Zheng L Cash VL Flint DH Dean DR 1998 Assembly of iron-sulfur clusters. Identification of an iscSUA-hscBA-fdx gene cluster from Azotobacter vinelandii J Biol Chem 273 13264 13272
63. Zheng M Wang X Templeton LJ Smulski DR LaRossa RA Storz G 2001 DNA microarray-mediated transcriptional profiling of the Escherichia coli response to hydrogen peroxide J Bacteriol 183 4562 4570