Home LiteratureArticle Details
PMID: 9791100 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't

Oxygen-insensitive nitroreductases: analysis of the roles of nfsA and nfsB in development of resistance to 5-nitrofuran derivatives in Escherichia coli.

Journal of bacteriology ·Vol. 180 ·No. 21 ·1998-11-00 ·Pages 5529-39

Whiteway J, Koziarz P, Veall J, Sandhu N, Kumar P, Hoecher B, Lambert IB

Abstract

Nitroheterocyclic and nitroaromatic compounds constitute an enormous range of chemicals whose potent biological activity has significant human health and environmental implications. The biological activity of nitro-substituted compounds is derived from reductive metabolism of the nitro moiety, a process catalyzed by a variety of nitroreductase activities. Resistance of bacteria to nitro-substituted compounds is believed to result primarily from mutations in genes encoding oxygen-insensitive nitroreductases. We have characterized the nfsA and nfsB genes of a large number of nitrofuran-resistant mutants of Escherichia coli and have correlated mutation with cell extract nitroreductase activity. Our studies demonstrate that first-step resistance to furazolidone or nitrofurazone results from an nfsA mutation, while the increased resistance associated with second-step mutants is a consequence of an nfsB mutation. Inferences made from mutation about the structure-function relationships of NfsA and NfsB are discussed, especially with regard to the identification of flavin mononucleotide binding sites. We show that expression of plasmid-carried nfsA and nfsB genes in resistant mutants restores sensitivity to nitrofurans. Among the 20 first-step and 53 second-step mutants isolated in this study, 65 and 49%, respectively, contained insertion sequence elements in nfsA and nfsB. IS1 integrated in both genes, while IS30 and IS186 were found only in nfsA and IS2 and IS5 were observed only in nfsB. Insertion hot spots for IS30 and IS186 are indicated in nfsA, and a hot spot for IS5 insertion is evident in nfsB. We discuss potential regional and sequence-specific determinants for insertion sequence element integration in nfsA and nfsB.

MeSH Terms
Amino Acid Sequence Base Sequence Cloning, Molecular Drug Resistance, Microbial Drug Resistance, Neoplasm Escherichia coli/drug effects,enzymology,genetics Escherichia coli Proteins Molecular Sequence Data Nitrofurans/pharmacology Nitroreductases/genetics,metabolism Oxygen Sequence Homology, Amino Acid
Chemicals
Escherichia coli Proteins Nitrofurans NfsA protein, E coli NfsB protein, E coli Nitroreductases Oxygen
Authors & Affiliations
7 authors, click to expand affiliations / ORCID
Whiteway J
Biology Department, Carleton University, Ottawa, Ontario, Canada K1S 5B6.
Koziarz P
Veall J
Sandhu N
Kumar P
Hoecher B
Lambert I B
References (78)
78 references, click to expand
  1. Effect of activated nitrofurans on DNA.
    Biochim Biophys Acta. 1975 Aug 21;402(2):142-9 PMID: 1100114
  2. Crystal structure of NADH oxidase from Thermus thermophilus.
    Nat Struct Biol. 1995 Dec;2(12):1109-14 PMID: 8846223
  3. The three-dimensional structure of NAD(P)H:quinone reductase, a flavoprotein involved in cancer chemoprotection and chemotherapy: mechanism of the two-electron reduction.
    Proc Natl Acad Sci U S A. 1995 Sep 12;92(19):8846-50 PMID: 7568029
  4. Mutagenicity of nitrofuran derivatives, including furylfuramide, a food preservative.
    Mutat Res. 1975;32(1):55-80 PMID: 124819
  5. Target site selection in transposition.
    Annu Rev Biochem. 1997;66:437-74 PMID: 9242914
  6. Determining the DNA sequence elements required for binding integration host factor to two different target sites.
    J Bacteriol. 1994 May;176(10):2999-3006 PMID: 8188600
  7. Biochemical characterization of NfsA, the Escherichia coli major nitroreductase exhibiting a high amino acid sequence homology to Frp, a Vibrio harveyi flavin oxidoreductase.
    J Bacteriol. 1996 Aug;178(15):4508-14 PMID: 8755878
  8. Nitrated polycyclic aromatic hydrocarbons: a risk assessment for the urban citizen.
    Environ Health Perspect. 1993 Oct;101 Suppl 3:309-15 PMID: 8143637
  9. Action of some nitrofuran derivatives on glucose metabolism, ATP levels, and macromolecule synthesis in Escherichia coli.
    Can J Microbiol. 1978 Jun;24(6):650-7 PMID: 352498
  10. The complete genome sequence of the gastric pathogen Helicobacter pylori.
    Nature. 1997 Aug 7;388(6642):539-47 PMID: 9252185
  11. The complete genome sequence of Escherichia coli K-12.
    Science. 1997 Sep 5;277(5331):1453-62 PMID: 9278503
  12. Purification and structural characterization of a flavoprotein induced by iron limitation in Methanobacterium thermoautotrophicum Marburg.
    J Bacteriol. 1995 May;177(9):2436-41 PMID: 7730275
  13. Genetics of nitrofurazone resistance in Escherichia coli.
    J Bacteriol. 1978 Jan;133(1):10-6 PMID: 338576
  14. 1,6-Dinitropyrene causes spindle disturbances and chromosomal damage in V79 Chinese hamster cells.
    Mutat Res. 1988 Jul;208(3-4):213-8 PMID: 3398871
  15. Conversion of NfsB, a minor Escherichia coli nitroreductase, to a flavin reductase similar in biochemical properties to FRase I, the major flavin reductase in Vibrio fischeri, by a single amino acid substitution.
    J Bacteriol. 1996 Aug;178(15):4731-3 PMID: 8755909
  16. Nonrandom location of IS1 elements in the genomes of natural isolates of Escherichia coli.
    Mol Biol Evol. 1997 Jul;14(7):725-32 PMID: 9214745
  17. Flavin mononucleotide-binding domain of the flavoprotein component of the sulfite reductase from Escherichia coli.
    Biochemistry. 1997 May 13;36(19):5921-8 PMID: 9153434
  18. Fast and sensitive multiple sequence alignments on a microcomputer.
    Comput Appl Biosci. 1989 Apr;5(2):151-3 PMID: 2720464
  19. Searching for and predicting the activity of sites for DNA binding proteins: compilation and analysis of the binding sites for Escherichia coli integration host factor (IHF).
    Nucleic Acids Res. 1990 Sep 11;18(17):4993-5000 PMID: 2205834
  20. Aerobic and anaerobic reduction of nitrated pyrenes in vitro.
    Chem Biol Interact. 1986 Oct 1;59(3):309-24 PMID: 3021349
  21. Metronidazole resistance in Helicobacter pylori is due to null mutations in a gene (rdxA) that encodes an oxygen-insensitive NADPH nitroreductase.
    Mol Microbiol. 1998 Apr;28(2):383-93 PMID: 9622362
  22. The nucleotide sequence and protein-coding capability of the transposable element IS5.
    Gene. 1981 Aug;14(3):155-63 PMID: 6269958
  23. Nitrofurantoin-resistant mutants of Escherichia coli: isolation and mapping.
    Mol Gen Genet. 1984;196(2):379-80 PMID: 6387400
  24. Physical characterisation of the Escherichia coli B gene encoding nitroreductase and its over-expression in Escherichia coli K12.
    FEMS Microbiol Lett. 1994 Dec 1;124(2):195-202 PMID: 7813889
  25. Escherichia coli integration host factor binds specifically to the ends of the insertion sequence IS1 and to its major insertion hot-spot in pBR322.
    J Mol Biol. 1987 May 20;195(2):261-72 PMID: 2821273
  26. Contribution of 1-nitropyrene to direct-acting Ames assay mutagenicities of diesel particulate extracts.
    Mutat Res. 1982 Apr;104(1-3):17-23 PMID: 6176864
  27. Cloning, nucleotide sequence, and expression of the nitroreductase gene from Enterobacter cloacae.
    J Biol Chem. 1991 Mar 5;266(7):4126-30 PMID: 1999406
  28. Does the insertion element IS1 transpose preferentially into A+T-rich DNA segments?
    Mol Gen Genet. 1980;178(2):471-3 PMID: 6248730
  29. IS186: an Escherichia coli insertion element isolated from a cDNA library.
    J Bacteriol. 1985 Nov;164(2):957-9 PMID: 2997142
  30. Genetic analyses of the interactions of the IS1-encoded proteins with the left end of IS1 and its insertion hotspot.
    J Mol Biol. 1997 Apr 4;267(3):548-60 PMID: 9126837
  31. The role of catalytic superoxide formation in the O2 inhibition of nitroreductase.
    Biochem Biophys Res Commun. 1975 Dec 15;67(4):1267-74 PMID: 173338
  32. A rapid boiling method for the preparation of bacterial plasmids.
    Anal Biochem. 1981 Jun;114(1):193-7 PMID: 6269464
  33. Identification of the gene encoding the major NAD(P)H-flavin oxidoreductase of the bioluminescent bacterium Vibrio fischeri ATCC 7744.
    J Bacteriol. 1994 Jun;176(12):3536-43 PMID: 8206830
  34. Purification and characterization of an oxygen-insensitive NAD(P)H nitroreductase from Enterobacter cloacae.
    J Biol Chem. 1991 Mar 5;266(7):4119-25 PMID: 1999405
  35. The pUC plasmids, an M13mp7-derived system for insertion mutagenesis and sequencing with synthetic universal primers.
    Gene. 1982 Oct;19(3):259-68 PMID: 6295879
  36. Mutations to nitrofurantoin and nitrofurazone resistance in Escherichia coli K12.
    J Gen Microbiol. 1983 Jan;129(1):99-103 PMID: 6339681
  37. Nucleotide sequence of Salmonella typhimurium nitroreductase gene.
    Nucleic Acids Res. 1990 Feb 25;18(4):1059 PMID: 2179862
  38. Chloramphenicol acetyltransferase from chloramphenicol-resistant bacteria.
    Methods Enzymol. 1975;43:737-55 PMID: 1094240
  39. Specificity of insertion of IS1.
    J Mol Biol. 1985 Oct 5;185(3):517-24 PMID: 2997452
  40. Characterization of the FAD binding domain of cytochrome P450 reductase.
    Arch Biochem Biophys. 1996 Jan 1;325(1):99-106 PMID: 8554349
  41. Flavin-binding and protein structural integrity studies on NADPH-cytochrome P450 reductase are consistent with the presence of distinct domains.
    Arch Biochem Biophys. 1995 Jan 10;316(1):267-74 PMID: 7840627
  42. Mutagenicity and carcinogenicity of nitroarenes and their sources in the environment.
    Crit Rev Toxicol. 1986;17(1):23-60 PMID: 2427276
  43. Mutation spectra of chemical fractions of a complex mixture: role of nitroarenes in the mutagenic specificity of municipal waste incinerator emissions.
    Mutat Res. 1996 Jan 17;349(1):1-20 PMID: 8569781
  44. The reduction of Furacin by cell-free extracts of Furacin-resistant and parent-susceptible strains of Escherichia coli.
    Arch Biochem Biophys. 1957 Jan;66(1):208-16 PMID: 13395540
  45. Basic local alignment search tool.
    J Mol Biol. 1990 Oct 5;215(3):403-10 PMID: 2231712
  46. Plasmid vectors for the selection of promoters.
    Gene. 1984 Feb;27(2):151-60 PMID: 6327464
  47. Reduction of Nitrated Diphenylamine Derivatives under Anaerobic Conditions.
    Appl Environ Microbiol. 1995 Sep;61(9):3282-7 PMID: 16535118
  48. Terminal inverted repeats of prokaryotic transposable element IS186 which can generate duplications of variable length at an identical target sequence.
    Gene. 1986;49(1):153-6 PMID: 3032747
  49. Escherichia coli integration host factor bends the DNA at the ends of IS1 and in an insertion hotspot with multiple IHF binding sites.
    EMBO J. 1987 Aug;6(8):2479-87 PMID: 2822395
  50. Oxygen-sensitive and -insensitive nitroreduction by Escherichia coli and rat hepatic microsomes.
    J Biol Chem. 1979 May 25;254(10):4009-14 PMID: 374406
  51. Flavin reductase P: structure of a dimeric enzyme that reduces flavin.
    Biochemistry. 1996 Oct 22;35(42):13531-9 PMID: 8885832
  52. Dichotomy in the mutagenicity and genotoxicity of nitropyrenes: apparent effect of the number of electrons involved in nitroreduction.
    Mutat Res. 1986 Jul;161(2):109-11 PMID: 3523222
  53. Nitropyrenes: isolation, identificaton, and reduction of mutagenic impurities in carbon black and toners.
    Science. 1980 Aug 29;209(4460):1039-43 PMID: 6996095
  54. Recalibrated linkage map of Escherichia coli K-12.
    Bacteriol Rev. 1976 Mar;40(1):116-67 PMID: 773363
  55. Characterization of the flavoprotein moieties of NADPH-sulfite reductase from Salmonella typhimurium and Escherichia coli. Physicochemical and catalytic properties, amino acid sequence deduced from DNA sequence of cysJ, and comparison with NADPH-cytochrome P-450 reductase.
    J Biol Chem. 1989 Sep 25;264(27):15796-808 PMID: 2550423
  56. DNA bending at adenine . thymine tracts.
    Nature. 1986 Apr 10-16;320(6062):501-6 PMID: 3960133
  57. Mode of action of nitrofurazone.
    J Bacteriol. 1970 Dec;104(3):1126-34 PMID: 16559085
  58. Mapping of insertion element IS30 in the Escherichia coli K12 chromosome.
    Mol Gen Genet. 1990 Jul;222(2-3):317-22 PMID: 1980336
  59. IS30, a new insertion sequence of Escherichia coli K12.
    Mol Gen Genet. 1984;196(1):68-73 PMID: 6090868
  60. Nucleotide sequences of the Acinetobacter calcoaceticus benABC genes for benzoate 1,2-dioxygenase reveal evolutionary relationships among multicomponent oxygenases.
    J Bacteriol. 1991 Sep;173(17):5385-95 PMID: 1885518
  61. Completion of the IS map in E. coli: IS186 positions on the E. coli K12 chromosome.
    Mol Gen Genet. 1991 Apr;226(1-2):318-20 PMID: 1851952
  62. Insertion sequence-related genetic variation in resting Escherichia coli K-12.
    Genetics. 1994 Mar;136(3):721-30 PMID: 7911771
  63. Estimation of wedge components in curved DNA.
    Nature. 1987 Apr 16-22;326(6114):720-2 PMID: 3561514
  64. Genetic studies on microbial cross resistance to toxic agents. I. Cross resistance of Escherichia coli to fifteen antibiotics.
    J Bacteriol. 1952 Oct;64(4):489-99 PMID: 12999676
  65. Bacterial insertion sequences.
    Curr Top Microbiol Immunol. 1996;204:1-26 PMID: 8556862
  66. Biodegradation of nitroaromatic compounds.
    Annu Rev Microbiol. 1995;49:523-55 PMID: 8561470
  67. Metabolism and biological effects of nitropyrene and related compounds.
    Res Rep Health Eff Inst. 1988 Feb;(16):1-22 PMID: 2855872
  68. Type I nitroreductases of Escherichia coli.
    Can J Microbiol. 1981 Jan;27(1):81-6 PMID: 7011517
  69. Characterization of an lrp-like (lrpC) gene from Bacillus subtilis.
    Mol Gen Genet. 1997 Sep;256(1):63-71 PMID: 9341680
  70. DNA curving and bending in protein-DNA recognition.
    Mol Microbiol. 1992 Sep;6(18):2549-55 PMID: 1333034
  71. Sequence-directed curvature of DNA.
    Annu Rev Biochem. 1990;59:755-81 PMID: 2197990
  72. Mutagen screening with bacteria: niridazole and nitrofurans.
    Mutat Res. 1975 Feb;31(1):31-7 PMID: 1093013
  73. The electron-transport proteins of hydroxylating bacterial dioxygenases.
    Annu Rev Microbiol. 1992;46:277-305 PMID: 1444257
  74. Mutagenesis and carcinogenesis by nitropyrenes and cancer chemotherapeutics. Meeting report.
    Mutat Res. 1986 Feb;164(1):3-8 PMID: 3512986
  75. Nitrofurazone-reducing enzymes in E. coli and their role in drug activation in vivo.
    Can J Microbiol. 1975 Oct;21(10):1484-91 PMID: 136
  76. Is the NAD(P)H:flavin oxidoreductase from Escherichia coli a member of the ferredoxin-NADP+ reductase family?. Evidence for the catalytic role of serine 49 residue.
    J Biol Chem. 1996 Jul 12;271(28):16656-61 PMID: 8663185
  77. Structural analysis of a new GC-specific insertion element IS186.
    FEBS Lett. 1985 Nov 11;192(1):47-52 PMID: 2996940
  78. Complete maps of IS1, IS2, IS3, IS4, IS5, IS30 and IS150 locations in Escherichia coli K12.
    Mol Gen Genet. 1989 Dec;220(1):147-53 PMID: 2558284
Article Info
Journal
Journal of bacteriology
Abbr.
J Bacteriol
ISSN
0021-9193
Published
1998-11-00
Pages
5529-39
Language
English
Region
United States
NLM ID
2985120R
PMCID
PMC107609
Subset
IM
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: product@genelibs.com