YcbX and yiiM, two novel determinants for resistance of Escherichia coli to N-hydroxylated base analogues

Molecular Microbiology

Volumn 68, Issue 1, 2008, Pages 51-65

  Kozmin, Stanislav G ^a,b   Leroy, Prune ^a,d   Pavlov, Youri I ^a,c   Schaaper, Roel M ^a  

^a NATIONAL INSTITUTE OF ENVIRONMENTAL HEALTH SCIENCES   (United States)

^b ST PETERSBURG STATE UNIVERSITY   (Russian Federation)

^c NEBRASKA MEDICAL CENTER   (United States)

^d UPPSALA UNIVERSITY   (Sweden)

Author keywords

[No Author keywords available]

Indexed keywords

6 N HYDROXYADENINE; ADENINE; BIOTIN; ESCHERICHIA COLI PROTEIN; FERREDOXIN; MUTANT PROTEIN; OXIDOREDUCTASE; PROTEIN MOSC; PROTEIN YCBX; PROTEIN YIIM; PURINE DERIVATIVE; SULFOXIDE; UNCLASSIFIED DRUG; XANTHINE DEHYDROGENASE;

AMINO ACID SEQUENCE; ANIMAL CELL; ANTIBIOTIC RESISTANCE; ARTICLE; BACTERIAL GENE; CONTROLLED STUDY; DETOXIFICATION; ENZYME ACTIVITY; ESCHERICHIA COLI; EUKARYOTIC CELL; GENETIC ANALYSIS; HYDROXYLATION; NONHUMAN; OPEN READING FRAME; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN ISOLATION; PROTEIN SYNTHESIS;

ESCHERICHIA COLI; EUKARYOTA;

EID: 40549106101     PISSN: 0950382X     EISSN: 13652958     Source Type: Journal    
DOI: 10.1111/j.1365-2958.2008.06128.x     Document Type: Article

References (61)

1. Amrani, L., Primus, J., Glatigny, A., Arcangeli, L., Scazzocchio, C., and Finnerty, V. (2000) Comparison of the sequences of the Aspergillus nidulans hxB and Drosophila melanogaster ma‐1 genes with nifS from Azotobacter vinelandii suggests a mechanism for the insertion of the terminal sulphur atom in the molybdopterin cofactor. Mol Microbiol 38: 114–125.
2. Anantharaman, V., and Aravind, L. (2002) MOSC domains: ancient, predicted sulfur‐carrier domains, present in diverse metal‐sulfur cluster biosynthesis proteins including Molybdenum cofactor sulfurases. FEMS Microbiol Lett 207: 55–61.
3. Angove, H.C., Cole, J.A., Richardson, D.J., and Butt, J.N. (2002) Protein film voltammetry reveals distinctive fingerprints of nitrite and hydroxylamine reduction by a cytochrome c nitrite reductase. J Biol Chem 277: 23374–23381.
4. Barrett, J.C. (1981) Induction of gene mutation in and cell transformation of mammalian cells by modified purines: 2‐aminopurine and 6‐ N ‐hydroxylaminopurine. Proc Natl Acad Sci USA 78: 5685–5689.
5. Berlyn, M.K.B. (1998) Linkage map of Escherichia coli K‐12, edition 10: the traditional map. Microbiol Mol Biol Rev 62: 814–984.
6. Bochner, B.R., and Savageau, M.A. (1977) Generalized indicator plate for genetic, metabolic, and taxonomic studies with microorganisms. Appl Environ Microbiol 33: 434–444.
7. Bochner, B.R., Gadzinski, P., and Panomitros, E. (2001) Phenotype microarrays for high‐throughput phenotypic testing and assay of gene function. Genome Res 11: 1246–1255.
8. Budowski, E.I. (1976) The mechanisms of the mutagenic action of hydroxylamine. Prog Nucleic Acid Res Mol Biol 16: 125–182.
9. Burgis, N.E., Brucker, J.J., and Cunningham, R.P. (2003) Repair system for noncanonical purines in Escherichia coli. J Bacteriol 185: 3101–3110.
10. Burgiss, N.E., and Cunningham, R.P. (2007) Substrate specificity of RdgB protein, a deoxyribonucleoside triphosphate pyrophosphohydrolase. J Biol Chem 282: 3531–3538.
11. Caetano‐Anolles, G. (1993) Amplifying DNA with arbitrary oligonucleotide primers. PCR Methods Appl 3: 85–94.
12. Del Campillo‐Campbell, A., and Campbell, A. (1982) Molybdenum cofactor requirement for biotin sulfoxide reduction in Escherichia coli. J Bacteriol 149: 469–478.
13. Clement, B., and Kunze, T. (1990) Hepatic microsomal N ‐hydroxylation of adenine to 6‐ N ‐hydroxylaminopurine. Biochem Pharmacol 39: 925–933.
14. Clement, B., and Kunze, T. (1992) The reduction of 6‐ N ‐hydroxylaminopurine to adenine by xanthine oxidase. Biochem Pharmacol 44: 1501–1509.
15. Dai, X., Hayashi, K., Nozaki, H., Cheng, Y., and Zhao, Y. (2005) Genetic and chemical analyses of the action mechanisms of sirtinol in Arabidopsis. Proc Natl Acad Sci USA 102: 3129–3134.
16. Datsenko, K.A., and Wanner, B.L. (2000) One‐step inactivation of chromosomal genes in Escherichia coli K‐12 using PCR products. Proc Natl Acad Sci USA 97: 6640–6645.
17. Elion, G.B. (1989) The purine path to chemotherapy. Science 244: 41–47.
18. Ezraty, B., Bos, J., Barras, F., and Aussel, L. (2005) Methionine sulfoxide reduction and assimilation in Escherichia coli: new role for the biotin sulfoxide reductase BisC. J Bacteriol 187: 231–237.
19. Freese, E. (1959) The specific mutagenic effect of base analogs on phage T4. J Mol Biol 1: 87–105.
20. Giner‐Sorolla, A., and Bendich, A. (1958) Synthesis and properties of some 6‐substituted purines. J Am Chem Soc 80: 3932–3937.
21. Havemeyer, A., Bittner, F., Wollers, S., Mendel, R., Kunze, T., and Clement, B. (2006) Identification of the missing component in the mitochondrial benzamidoxime prodrug converting system as a novel molybdenum enzyme. J Biol Chem 281: 34796–34802.
22. Hille, R. (2002) Molybdenum and tungsten in biology. Trends Biochem Sci 27: 360–367.
23. Hwang, K.Y., Chung, J.H., Kim, S.H., Han, Y.S., and Cho, Y. (1999) Structure‐based identification of a novel NTPase from Methanococcus jannaschii. Nat Struct Biol 6: 691–696.
24. Janion, C. (1978) The efficiency and extent of mutagenic activity of some new mutagens of base‐analogue type. Mutat Res 56: 225–234.
25. Janion, C. (1979) On the different response of Salmonella typhimurium hisG46 and TA1530 to mutagenic action of base analogues. Acta Biochim Pol 26: 171–177.
26. Janion, C., and Myszkowska, K. (1981) Mutagenic and inhibitory properties of some new purine analogs on Salmonella typhimurium TA1530. Mutat Res 91: 193–197.
27. Khromov‐Borisov, N.N. (1997) Naming the mutagenic nucleic acid base analogs: the Galatea syndrome. Mutat Res 379: 95–103.
28. Kisker, C., Schindelin, H., Baas, D., Retey, J., Meckenstock, R.U., and Kroneck, P.M. (1999) A structural comparison of molybdenum cofactor‐containing enzymes. FEMS Microbiol Rev 22: 503–521.
29. Kleckner, N., Bender, J., and Gottesman. S. (1991) Uses of transposons with emphasis on Tn 10. Methods Enzymol 204: 139–180.
30. Kozmin, S.G., and Schaaper, R.M. (2007) Molybdenum cofactor‐dependent resistance to N ‐hydroxylated base analogs in E. coli is independent of MobA function. Mutat Res 619: 9–15.
31. Kozmin, S.G., Schaaper, R.M., Shcherbakova, P.V., Kulikov, V.N., Noskov, V.N., Guetsova, M.L., et al. (1998a) Multiple antimutagenesis mechanisms affect mutagenic activity and specificity of the base analog 6‐ N ‐hydroxylaminopurine in bacteria and yeast. Mutat Res 402: 41–50.
32. Kozmin, S.G., Leroy, P., and Pavlov, Y.I. (1998b) Overexpression of the yeast HAM1 gene prevents 6‐ N ‐hydroxylaminopurine mutagenesis in Escherichia coli. Acta Biochim Pol 45: 645–652.
33. Kozmin, S.G., Pavlov, Y.I., Dunn, R.L., and Schaaper, R.M. (2000) Hypersensitivity of Escherichia coli Δ(uvrB‐bio) mutants to 6‐hydroxylaminopurine and other base analogs is due to a defect in molybdenum cofactor biosynthesis. J Bacteriol 182: 3361–3367.
34. Lieberman, I. (1956) Enzymatic synthesis of adenosine‐5′‐phosphate from inosine‐5′‐phosphate. J Biol Chem 223: 327–339.
35. Lu, A.L., Clark, S., and Modrich, P. (1983) Methyl‐directed repair of DNA base‐pair mismatches in vitro. Proc Natl Acad Sci USA 80: 4639–4643.
36. Marchler‐Bauer, A., Anderson, J.B., Cherukuri, P.F., DeWeese‐Scott, C., Geer, L.Y., Gwadz, M., et al. (2005) CDD: a conserved domain database for protein classification. Nucleic Acids Res 33: D192–D196.
37. Matsui, H., Shimaoka, M., Kawaski, H., Takenaka, Y., and Kurahashi, O. (2001) Adenine deaminase activity of the yicP gene product of Escherichia coli. Biosci Biotechnol Biochem 65: 1112–1118.
38. Mendel, R.R., and Bittner, F. (2006) Cell biology of molybdenum. Biochim Biophys Acta 1763: 621–635.
39. Miller, J.H. (1972) Experiments in Molecular Genetics. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory.
40. Noskov, V.N., Staak, K., Shcherbakova, P.V., Kozmin, S.G., Negishi, K., Ono, B.‐C., et al. (1996) HAM1, the gene controlling 6‐ N ‐hydroxylaminopurine sensitivity and mutagenesis in the yeast Saccharomyces cerevisiae. Yeast 12: 17–29.
41. Pavlov, Y.I. (1986) Saccharomyces cerevisiae mutants highly sensitive to the mutagenic action of 6‐ N ‐hydroxylaminopurine. Genetika 22: 1099–1107.
42. Pavlov, Y.I., Noskov, V.N., Lange, E.K., Moiseeva, E.V., Pshenichnov, M.R., and Khromov‐Borisov, N.N. (1991) The genetic activity of N 6 ‐hydroxyadenine and 2‐amino‐ N 6 ‐hydroxyadenine in Escherichia coli, Salmonella typhimurium and Saccharomyces cerevisiae. Mutat Res 253: 33–46.
43. Pavlov, Y.I., Suslov, V.V., Shcherbakova, P.V., Kunkel, T.A., Ono, A., Matsuda, A., and Schaaper, R.M. (1996) Base analog N6 ‐hydroxylaminopurine mutagenesis in Escherichia coli: genetic control and molecular specificity. Mutat Res 357: 1–15.
44. Peretz, H., Naamati, M.S., Levartovsky, D., Lagziel, A., Shani, E., Horn, I., et al. (2007) Identification and characterization of the first mutation (Arg776Cys) in the C‐terminal domain of the human molybdenum cofactor sulfurase (HMCS) associated with type II classical xanthinuria. Mol Genet Metab 91: 23–29.
45. Pierson, D.E., and Campbell, A. (1990) Cloning and nucleotide sequence of bisC, the structural gene for biotin sulfoxide reductase in Escherichia coli. J Bacteriol 172: 2194–2198.
46. Pollock, V.V., and Barber, M.J. (1997) Biotin sulfoxide reductase. Heterologous expression and characterization of a functional molybdopterin guanine dinucleotide‐containing enzyme. J Biol Chem 272: 3355–3362.
47. Popowska, E., and Janion, C. (1975) The metabolism of N 4 ‐hydroxycytidine–a mutagen for Salmonella typhimurium. Nucleic Acids Res 2: 1143–1152.
48. Popowska, E., and Janion, C. (1977) The N 4 ‐hydroxycytidine reduction system in toluenized cells of Salmonella typhimurium. Acta Biochim Pol 24: 197–205.
49. Rajagopalan, K.V. (1996) Biosynthesis of the molybdenum cofactor. In Neidhardt, F.C. (ed). Escherichia coli and Salmonella: Cellular and Molecular Biology. Washington, DC: American Society for Microbiology Press, pp. 674–679.
50. Rosenkranz, H.S., and Mermelstein, R. (1983) Mutagenicity and genotoxicity of nitroarenes. All nitro‐containing chemicals were not created equal. Mutat Res 114: 217–267.
51. Sagi, M., Scazzocchio, C., and Fluhr, R. (2002) The absence of molybdenum cofactor sulfuration is the primary cause of the flacca phenotype in tomato plants. Plant J 31: 305–317.
52. Schaaper, R.M., Danforth, B.N., and Glickman, B.W. (1985) Rapid repeated cloning of mutant lac repressor genes. Gene 39: 181–189.
53. Shanmugam, K.T., Stewart, V., Gunsalus, R.P., Boxer, D.H., Cole, J.A., Chippaux, M., et al. (1992) Proposed nomenclature for the genes involved in molybdenum metabolism in Escherichia coli and Salmonella typhimurium. Mol Microbiol 6: 3452–3454.
54. Simandan, T., Sun, J., and Dix, T.A. (1998) Oxidation of DNA bases, deoxyribonucleosides and homopolymerase by peroxyl radicals. Biochem J 335: 233–240.
55. Stewart, V., and MacGregor, C.H. (1982) Nitrate reductase in Escherichia coli K‐12: involvement of chlC, chlE, and chlG loci. J Bacteriol 151: 788–799.
56. Sticht, H., and Rösch, P. (1998) The structure of iron‐sulfur proteins. Prog Biophys Mol Biol 70: 95–136.
57. Studier, F.W., and Moffatt, B.A. (1986) Use of bacteriophage T7 RNA polymerase to direct selective high‐level expression of cloned genes. J Mol Biol 189: 113–130.
58. Vogel, H.J., and Bonner, D.M. (1956) Acetylornithinase of Escherichia coli: partial purification and some properties. J Biol Chem 218: 97–106.
59. Wolfe, M.T., Heo, J., Garavelli, J.S., and Ludden, P.W. (2002) Hydroxylamine reductase activity of the hybrid cluster protein from Escherichia coli. J Bacteriol 184: 5898–5902.
60. Xi, H., Schneider, B.L., and Reitzer, L. (2000) Purine catabolism in Escherichia coli and function of xanthine dehydrogenase in purine salvage. J Bacteriol 182: 5332–5341.
61. Zalkin, H., and Nygaard, P. (1996) Biosynthesis of purine nucleotides. In Neidhardt, F.C. (ed). Escherichia Coli and Salmonella: Cellular and Molecular Biology. Washington, DC: American Society for Microbiology Press, pp. 561–579.