Helicobacter hepaticus NikR controls urease and hydrogenase activities via the NikABDE and HH0418 putative nickel import proteins

Microbiology (United Kingdom)

Volumn 159, Issue 1, 2013, Pages 136-146

  Benoit, Stéphane L ^a   Seshadri, Susmitha ^a   Lamichhane Khadka, Reena ^a,b   Maier, Robert J ^a  

^a UNIVERSITY OF GEORGIA   (United States)

^b SAINT MARY'S COLLEGE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN; ERYTHROMYCIN; HYDROGENASE; NICKEL; PROTEIN ABDE; PROTEIN HH0418; UNCLASSIFIED DRUG; UREASE;

ARTICLE; BACTERIAL STRAIN; CYTOPLASM; ENZYME ACTIVITY; ENZYME BINDING; ENZYME REGULATION; GENE CASSETTE; GENE DISRUPTION; HELICOBACTER HEPATICUS; HELICOBACTER PYLORI; PRIORITY JOURNAL;

AMINO ACID SEQUENCE; BASE SEQUENCE; DNA, BACTERIAL; ELECTROPHORETIC MOBILITY SHIFT ASSAY; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, BACTERIAL; GENE KNOCKOUT TECHNIQUES; HELICOBACTER HEPATICUS; HYDROGENASE; MEMBRANE TRANSPORT PROTEINS; MOLECULAR SEQUENCE DATA; MUTAGENESIS, INSERTIONAL; NICKEL; PROMOTER REGIONS, GENETIC; PROTEIN BINDING; REAL-TIME POLYMERASE CHAIN REACTION; REPRESSOR PROTEINS; UREASE;

HELICOBACTER HEPATICUS; HELICOBACTER PYLORI;

EID: 84871704039     PISSN: 13500872     EISSN: None     Source Type: Journal    
DOI: 10.1099/mic.0.062976-0     Document Type: Article

References (48)

1. Alm, R. A., Ling, L. S., Moir, D. T., King, B. L., Brown, E. D., Doig, P. C., Smith, D. R., Noonan, B., Guild, B. C. & other authors (1999). Genomic-sequence comparison of two unrelated isolates of the human gastric pathogen Helicobacter pylori. Nature 397, 176-180.
2. Beckwith, C. S., McGee, D. J., Mobley, H. L. & Riley, L. K. (2001). Cloning, expression, and catalytic activity of Helicobacter hepaticus urease. Infect Immun 69, 5914-5920.
3. Belzer, C., Stoof, J., Beckwith, C. S., Kuipers, E. J., Kusters, J. G. & van Vliet, A. H. (2005). Differential regulation of urease activity in Helicobacter hepaticus and Helicobacter pylori. Microbiology 151, 3989-3995.
4. Belzer, C., Stoof, J. & van Vliet, A. H. M. (2007a). Metal-responsive gene regulation and metal transport in Helicobacter species. Biometals 20, 417-429.
5. Belzer, C., van Schendel, B. A., Kuipers, E. J., Kusters, J. G. & van Vliet, A. H. (2007b). Iron-responsive repression of urease expression in Helicobacter hepaticus is mediated by the transcriptional regulator Fur. Infect Immun 75, 745-752.
6. Benanti, E. L. & Chivers, P. T. (2007). The N-terminal arm of the Helicobacter pylori Ni2+-dependent transcription factor NikR is required for specific DNA binding. J Biol Chem 282, 20365-20375.
7. Benanti, E. L. & Chivers, P. T. (2010). Geobacter uraniireducens NikR displays a DNA binding mode distinct from other members of the NikR family. J Bacteriol 192, 4327-4336.
8. Benoit, S. L. & Maier, R. J. (2008). Hydrogen and nickel metabolism in helicobacter species. Ann N Y Acad Sci 1125, 242-251.
9. Benoit, S. L., Zbell, A. L. & Maier, R. J. (2007). Nickel enzyme maturation in Helicobacter hepaticus: roles of accessory proteins in hydrogenase and urease activities. Microbiology 153, 3748-3756.
10. Bloom, S. L. & Zamble, D. B. (2004). Metal-selective DNA-binding response of Escherichia coli NikR. Biochemistry 43, 10029-10038.
11. Chen, Y. Y. & Burne, R. A. (2003). Identification and characterization of the nickel uptake system for urease biogenesis in Streptococcus salivarius 57.I. J Bacteriol 185, 6773-6779.
12. Chivers, P. T. & Sauer, R. T. (1999). NikR is a ribbon-helix-helix DNA-binding protein. Protein Sci 8, 2494-2500.
13. Chivers, P. T. & Sauer, R. T. (2000). Regulation of high affinity nickel uptake in bacteria. Ni2+-Dependent interaction of NikR with wildtype and mutant operator sites. J Biol Chem 275, 19735-19741.
14. Chivers, P. T. & Sauer, R. T. (2002). NikR repressor: high-affinity nickel binding to the C-terminal domain regulates binding to operator DNA. Chem Biol 9, 1141-1148.
15. Contreras, M., Thiberge, J. M., Mandrand-Berthelot, M. A. & Labigne, A. (2003). Characterization of the roles of NikR, a nickel-responsive pleiotropic autoregulator of Helicobacter pylori. Mol Microbiol 49, 947-963.
16. Danielli, A. & Scarlato, V. (2010). Regulatory circuits in Helicobacter pylori network motifs and regulators involved in metal-dependent responses. FEMS Microbiol Rev 34, 738-752.
17. Davis, G. S., Flannery, E. L. & Mobley, H. L. (2006). Helicobacter pylori HP1512 is a nickel-responsive NikR-regulated outer membrane protein. Infect Immun 74, 6811-6820.
18. De Pina, K., Desjardin, V., Mandrand-Berthelot, M. A., Giordano, G. & Wu, L. F. (1999). Isolation and characterization of the nikR gene encoding a nickel-responsive regulator in Escherichia coli. J Bacteriol 181, 670-674.
19. Delany, I., Ieva, R., Soragni, A., Hilleringmann, M., Rappuoli, R. & Scarlato, V. (2005). In vitro analysis of protein-operator interactions of the NikR and fur metal-responsive regulators of coregulated genes in Helicobacter pylori. J Bacteriol 187, 7703-7715.
20. Dosanjh, N. S. & Michel, S. L. (2006). Microbial nickel metalloregulation: NikRs for nickel ions. Curr Opin Chem Biol 10, 123-130.
21. Dosanjh, N. S., Hammerbacher, N. A. & Michel, S. L. (2007). Characterization of the Helicobacter pylori NikR-P(ureA) DNA interaction: metal ion requirements and sequence specificity. Biochemistry 46, 2520-2529.
22. Dosanjh, N. S., West, A. L. & Michel, S. L. (2009). Helicobacter pylori NikR's interaction with DNA: a two-tiered mode of recognition. Biochemistry 48, 527-536.
23. Eitinger, T. & Mandrand-Berthelot, M. A. (2000). Nickel transport systems in microorganisms. Arch Microbiol 173, 1-9.
24. Eppinger, M., Baar, C., Linz, B., Raddatz, G., Lanz, C., Keller, H., Morelli, G., Gressmann, H., Achtman, M. & Schuster, S. C. (2006). Who ate whom? Adaptive Helicobacter genomic changes that accompanied a host jump from early humans to large felines. PLoS Genet 2, e120.
25. Ernst, F. D., Stoof, J., Horrevoets, W. M., Kuipers, E. J., Kusters, J. G. & van Vliet, A. H. (2006). NikR mediates nickel-responsive transcriptional repression of the Helicobacter pylori outer membrane proteins FecA3 (HP1400) and FrpB4 (HP1512). Infect Immun 74, 6821-6828.
26. Evans, S. E. & Michel, S. L. (2012). Dissecting the role of DNA sequence in Helicobacter pylori NikR/DNA recognition. Dalton Trans 41, 7946-7951.
27. Ge, R., Watt, R. M., Sun, X., Tanner, J. A., He, Q. Y., Huang, J. D. & Sun, H. (2006). Expression and characterization of a histidine-rich protein, Hpn: potential for Ni2+ storage in Helicobacter pylori. Biochem J 393, 285-293.
28. Ge, Z., Lee, A., Whary, M. T., Rogers, A. B., Maurer, K. J., Taylor, N. S., Schauer, D. B. & Fox, J. G. (2008). Helicobacter hepaticus urease is not required for intestinal colonization but promotes hepatic inflammation in male A/JCr mice. Microb Pathog 45, 18-24.
29. Hughes, K. T., Ladika, D., Roth, J. R. & Olivera, B. M. (1983). An indispensable gene for NAD biosynthesis in Salmonella typhimurium. J Bacteriol 155, 213-221.
30. Maier, R. J., Fu, C., Gilbert, J., Moshiri, F., Olson, J. & Plaut, A. G. (1996). Hydrogen uptake hydrogenase in Helicobacter pylori. FEMS Microbiol Lett 141, 71-76.
31. Mehta, N. S., Benoit, S., Mysore, J. V., Sousa, R. S. & Maier, R. J. (2005). Helicobacter hepaticus hydrogenase mutants are deficient in hydrogen-supported amino acid uptake and in causing liver lesions in A/J mice. Infect Immun 73, 5311-5318.
32. Mehta, N. S., Benoit, S. L., Mysore, J. & Maier, R. J. (2007). In vitro and in vivo characterization of alkyl hydroperoxide reductase mutant strains of Helicobacter hepaticus. Biochim Biophys Acta 1770, 257-265.
33. Mobley, H. L., Garner, R. M. & Bauerfeind, P. (1995). Helicobacter pylori nickel-transport gene nixA: synthesis of catalytically active urease in Escherichia coli independent of growth conditions. Mol Microbiol 16, 97-109.
34. Mulrooney, S. B. & Hausinger, R. P. (2003). Nickel uptake and utilization by microorganisms. FEMS Microbiol Rev 27, 239-261.
35. Oh, J. D., Kling-Bäckhed, H., Giannakis, M., Xu, J., Fulton, R. S., Fulton, L. A., Cordum, H. S., Wang, C., Elliott, G. & other authors (2006). The complete genome sequence of a chronic atrophic gastritis Helicobacter pylori strain: evolution during disease progression. Proc Natl Acad Sci U S A 103, 9999-10004.
36. Romagnoli, S., Agriesti, F. & Scarlato, V. (2011). In vivo recognition of the fecA3 target promoter by Helicobacter pylori NikR. J Bacteriol 193, 1131-1141.
37. Schauer, K., Gouget, B., Carrière, M., Labigne, A. & de Reuse, H. (2007). Novel nickel transport mechanism across the bacterial outer membrane energized by the TonB/ExbB/ExbD machinery. Mol Microbiol 63, 1054-1068.
38. Schauer, K., Muller, C., Carrière, M., Labigne, A., Cavazza, C. & De Reuse, H. (2010). The Helicobacter pylori GroES cochaperonin HspA functions as a specialized nickel chaperone and sequestration protein through its unique C-terminal extension. J Bacteriol 192, 1231-1237.
39. Schreiter, E. R., Sintchak, M. D., Guo, Y., Chivers, P. T., Sauer, R. T. & Drennan, C. L. (2003). Crystal structure of the nickel-responsive transcription factor NikR. Nat Struct Biol 10, 794-799.
40. Seshadri, S., Benoit, S. L. & Maier, R. J. (2007). Roles of His-rich hpn and hpn-like proteins in Helicobacter pylori nickel physiology. J Bacteriol 189, 4120-4126.
41. Stähler, F. N., Odenbreit, S., Haas, R., Wilrich, J., van Vliet, A. H. M., Kusters, J. G., Kist, M. & Bereswill, S. (2006). The novel Helicobacter pylori CznABC metal efflux pump is required for cadmium, zinc, and nickel resistance, urease modulation, and gastric colonization. Infect Immun 74, 3845-3852.
42. Stoof, J., Kuipers, E. J., Klaver, G. & van Vliet, A. H. (2010a). An ABC transporter and a TonB ortholog contribute to Helicobacter mustelae nickel and cobalt acquisition. Infect Immun 78, 4261-4267.
43. Stoof, J., Kuipers, E. J. & van Vliet, A. H. M. (2010b). Characterization of NikR-responsive promoters of urease and metal transport genes of Helicobacter mustelae. Biometals 23, 145-159.
44. Suerbaum, S., Josenhans, C., Sterzenbach, T., Drescher, B., Brandt, P., Bell, M., Droge, M., Fartmann, B., Fischer, H. P. & other authors (2003). The complete genome sequence of the carcinogenic bacterium Helicobacter hepaticus. Proc Natl Acad Sci U S A 100, 7901-7906.
45. Tomb, J. F., White, O., Kerlavage, A. R., Clayton, R. A., Sutton, G. G., Fleischmann, R. D., Ketchum, K. A., Klenk, H. P., Gill, S. & other authors (1997). The complete genome sequence of the gastric pathogen Helicobacter pylori. Nature 388, 539-547.
46. Wang, S. C., Li, Y., Robinson, C. V. & Zamble, D. B. (2010). Potassium is critical for the Ni(II)-responsive DNA-binding activity of Escherichia coli NikR. J Am Chem Soc 132, 1506-1507.
47. Weatherburn, M. W. (1967). Phenol-hypochlorite reaction for determination of ammonia. Anal Chem 39, 971-974.
48. West, A. L., Evans, S. E., González, J. M., Carter, L. G., Tsuruta, H., Pozharski, E. & Michel, S. L. (2012). Ni(II) coordination to mixed sites modulates DNA binding of HpNikR via a long-range effect. Proc Natl Acad Sci U S A 109, 5633-5638.