An ABC transporter and a TonB ortholog contribute to Helicobacter mustelae nickel and cobalt acquisition

Infection and Immunity

Volumn 78, Issue 10, 2010, Pages 4261-4267

  Stoof, Jeroen ^a,d   Kuipers, Ernst J ^a   Klaver, Gerard ^b   Van Vliet, Arnoud H M ^a,c  

^a ERASMUS MEDICAL CENTER   (Netherlands)

^b TNO   (Netherlands)

^c INSTITUTE OF FOOD RESEARCH   (United Kingdom)

^d UNIVERSITY OF NOTTINGHAM   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ABC TRANSPORTER; COBALT; FERRIC UPTAKE REGULATOR; HEME; IRON; NICKEL; OUTER MEMBRANE PROTEIN; PROTEIN TONB1; PROTEIN TONB2; UNCLASSIFIED DRUG; UREASE;

ARTICLE; BACTERIAL GENOME; CEUE GENE; FECD GENE; FRPB2 GENE; GENE EXPRESSION; GENE MUTATION; HELICOBACTER MUSTELAE; NIXA GENE; NONHUMAN; PRIORITY JOURNAL; TONB1 GENE; TONB2 GENE;

ANIMALS; ATP-BINDING CASSETTE TRANSPORTERS; BACTERIAL PROTEINS; BIOLOGICAL TRANSPORT; COBALT; FERRETS; GENE EXPRESSION REGULATION, BACTERIAL; GENOME, BACTERIAL; HELICOBACTER MUSTELAE; MEMBRANE PROTEINS; MUTATION; NICKEL; UREASE;

EID: 77957739195     PISSN: 00199567     EISSN: 10985522     Source Type: Journal    
DOI: 10.1128/IAI.00365-10     Document Type: Article

References (48)

1. Andrews, S. C., A. K. Robinson, and F. Rodriguez-Quinones. 2003. Bacterial iron homeostasis. FEMS Microbiol. Rev. 27:215-237.
2. Andrutis, K. A., J. G. Fox, D. B. Schauer, R. P. Marini, J. C. Murphy, L. Yan, and J. V. Solnick. 1995. Inability of an isogenic urease-negative mutant stain of Helicobacter mustelae to colonize the ferret stomach. Infect. Immun. 63:3722-3725.
3. Belzer, C., J. Stoof, C. S. Beckwith, E. J. Kuipers, J. G. Kusters, and A. H. M. van Vliet. 2005. Differential regulation of urease activity in Helicobacter hepaticus and Helicobacter pylori. Microbiology 151:3989-3995.
4. Belzer, C., J. Stoof, and A. H. M. van Vliet. 2007. Metal-responsive gene regulation and metal transport in Helicobacter species. Biometals 20:417-429.
5. Bruggraber, S. F., G. French, R. P. Thompson, and J. J. Powell. 2004. Selective and effective bactericidal activity of the cobalt (II) cation against Helicobacter pylori. Helicobacter 9:422-428.
6. Cavet, J. S., W. Meng, M. A. Pennella, R. J. Appelhoff, D. P. Giedroc, and N. J. Robinson. 2002. A nickel-cobalt-sensing ArsR-SmtB family repressor. Contributions of cytosol and effector binding sites to metal selectivity. J. Biol. Chem. 277:38441-38448.
7. Contreras, M., J. M. Thiberge, M. A. Mandrand-Berthelot, and A. Labigne. 2003. Characterization of the roles of NikR, a nickel-responsive pleiotropic autoregulator of Helicobacter pylori. Mol. Microbiol. 49:947-963. (Pubitemid 36981341)
8. Croinin, T. O., A. McCormack, A. H. M. van Vliet, J. G. Kusters, and B. Bourke. 2007. Random mutagenesis to identify novel Helicobacter mustelae virulence factors. FEMS Immunol. Med. Microbiol. 50:257-263.
9. Danielli, A., S. Romagnoli, D. Roncarati, L. Costantino, I. Delany, and V. Scarlato. 2009. Growth phase and metal-dependent transcriptional regulation of the fecA genes in Helicobacter pylori. J. Bacteriol. 191:3717-3725.
10. Davis, G. S., E. L. Flannery, and H. L. Mobley. 2006. Helicobacter pylori HP1512 is a nickel-responsive NikR-regulated outer membrane protein. Infect. Immun. 74:6811-6820.
11. Dhaenens, L., F. Szczebara, S. Van Nieuwenhuyse, and M. O. Husson. 1999. Comparison of iron uptake in different Helicobacter species. Res. Microbiol. 150:475-481.
12. Eppinger, M., C. Baar, B. Linz, G. Raddatz, C. Lanz, H. Keller, G. Morelli, H. Gressmann, M. Achtman, and S. C. Schuster. 2006. Who ate whom? Adaptive Helicobacter genomic changes that accompanied a host jump from early humans to large felines. PLoS Genet. 2:e120.
13. Ernst, F. D., S. Bereswill, B. Waidner, J. Stoof, U. Mader, J. G. Kusters, E. J. Kuipers, M. Kist, A. H. M. van Vliet, and G. Homuth. 2005. Transcriptional profiling of Helicobacter pylori Fur- and iron-regulated gene expression. Microbiology 151:533-546.
14. Ernst, F. D., J. Stoof, W. M. Horrevoets, E. J. Kuipers, J. G. Kusters, and A. H. M. van Vliet. 2006. NikR mediates nickel-responsive transcriptional repression of the Helicobacter pylori outer membrane proteins FecA3 (HP1400) and FrpB4 (HP1512). Infect. Immun. 74:6821-6828.
15. Gancz, H., S. Censini, and D. S. Merrell. 2006. Iron and pH homeostasis intersect at the level of Fur regulation in the gastric pathogen Helicobacter pylori. Infect. Immun. 74:602-614.
16. Haas, R., A. F. Kahrs, D. Facius, H. Allmeier, R. Schmitt, and T. F. Meyer. 1993. TnMax - a versatile mini-transposon for the analysis of cloned genes and shuttle mutagenesis. Gene 130:23-31.
17. Kusters, J. G., A. H. M. van Vliet, and E. J. Kuipers. 2006. Pathogenesis of Helicobacter pylori infection. Clin. Microbiol. Rev. 19:449-490.
18. Mulrooney, S. B., and R. P. Hausinger. 2003. Nickel uptake and utilization by microorganisms. FEMS Microbiol. Rev. 27:239-261.
19. Nolan, K. J., D. J. McGee, H. M. Mitchell, T. Kolesnikow, J. M. Harro, J. O'Rourke, J. E. Wilson, S. J. Danon, N. D. Moss, H. L. Mobley, and A. Lee. 2002. In vivo behavior of a Helicobacter pylori SS1 nixA mutant with reduced urease activity. Infect. Immun. 70:685-691.
20. Olson, J. W., and R. J. Maier. 2002. Molecular hydrogen as an energy source for Helicobacter pylori. Science 298:1788-1790.
21. O'Rourke, J. L., and A. Lee. 2003. Animal models of Helicobacter pylori infection and disease. Microbes Infect. 5:741-748.
22. O'Toole, P. W., W. J. Snelling, C. Canchaya, B. M. Forde, K. R. Hardie, C. Josenhans, R. L. Graham, G. McMullan, J. Parkhill, E. Belda, and S. D. Bentley. 2010. Comparative genomics and proteomics of Helicobacter mustelae, an ulcerogenic and carcinogenic gastric pathogen. BMC Genomics 11:164.
23. Outten, C. E., and T. V. O'Halloran. 2001. Femtomolar sensitivity of metalloregulatory proteins controlling zinc homeostasis. Science 292:2488-2492.
24. Pflock, M., S. Kennard, N. Finsterer, and D. Beier. 2006. Acid-responsive gene regulation in the human pathogen Helicobacter pylori. J. Biotechnol. 126:52-60.
25. Pot, R. G., J. Stoof, P. J. Nuijten, L. A. de Haan, P. Loeffen, E. J. Kuipers, A. H. M. van Vliet, and J. G. Kusters. 2007. UreA2B2: a second urease system in the gastric pathogen Helicobacter felis. FEMS Immunol. Med. Microbiol. 50:273-279.
26. Rodionov, D. A., P. Hebbeln, M. S. Gelfand, and T. Eitinger. 2006. Comparative and functional genomic analysis of prokaryotic nickel and cobalt uptake transporters: evidence for a novel group of ATP-binding cassette transporters. J. Bacteriol. 188:317-327.
27. Sambrook, J., E. F. Fritsch, and T. Maniatis. 1989. Molecular cloning: a laboratory manual, 2nd ed. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
28. Schauer, K., B. Gouget, M. Carriere, A. Labigne, and H. de Reuse. 2007. Novel nickel transport mechanism across the bacterial outer membrane energized by the TonB/ExbB/ExbD machinery. Mol. Microbiol. 63:1054-1068.
29. Schauer, K., D. A. Rodionov, and H. de Reuse. 2008. New substrates for TonB-dependent transport: do we only see the 'tip of the iceberg'? Trends Biochem. Sci. 33:330-338.
30. Senkovich, O., S. Ceaser, D. J. McGee, and T. L. Testerman. 2010. Unique host iron utilization mechanisms of Helicobacter pylori revealed using iron-deficient chemically defined media. Infect. Immun. 78:1841-1849.
31. Solnick, J. V., and D. B. Schauer. 2001. Emergence of diverse Helicobacter species in the pathogenesis of gastric and enterohepatic diseases. Clin. Microbiol. Rev. 14:59-97.
32. Stingl, K., and H. De Reuse. 2005. Staying alive overdosed: how does Helicobacter pylori control urease activity? Int. J. Med. Microbiol. 295:307-315.
33. Stoof, J., S. Breijer, R. G. Pot, D. van der Neut, E. J. Kuipers, J. G. Kusters, and A. H. M. van Vliet. 2008. Inverse nickel-responsive regulation of two urease enzymes in the gastric pathogen Helicobacter mustelae. Environ. Microbiol. 10:2586-2597.
34. Stoof, J., E. J. Kuipers, and A. H. M. van Vliet. 2010. Characterization of NikR-responsive promoters of urease and metal transport genes of Helicobacter mustelae. Biometals 23:145-159.
35. Tomb, J. F., O. White, A. R. Kerlavage, R. A. Clayton, G. G. Sutton, R. D. Fleischmann, K. A. Ketchum, H. P. Klenk, S. Gill, B. A. Dougherty, K. Nelson, J. Quackenbush, L. Zhou, E. F. Kirkness, S. Peterson, et al. 1997. The complete genome sequence of the gastric pathogen Helicobacter pylori. Nature 388:539-547.
36. Tree, J. J., S. P. Kidd, M. P. Jennings, and A. G. McEwan. 2005. Copper sensitivity of cueO mutants of Escherichia coli K-12 and the biochemical suppression of this phenotype. Biochem. Biophys. Res. Commun. 328:1205-1210.
37. Tsuda, M., M. Karita, M. G. Morshed, K. Okita, and T. Nakazawa. 1994. A urease-negative mutant of Helicobacter pylori constructed by allelic exchange mutagenesis lacks the ability to colonize the nude mouse stomach. Infect. Immun. 62:3586-3589.
38. van Vliet, A. H. M., F. D. Ernst, and J. G. Kusters. 2004. NikR-mediated regulation of Helicobacter pylori acid-adaptation. Trends Microbiol. 12:489-494.
39. van Vliet, A. H. M., J. Stoof, R. Vlasblom, S. A. Wainwright, N. J. Hughes, D. J. Kelly, S. Bereswill, J. J. Bijlsma, T. Hoogenboezem, C. M. Vandenbroucke-Grauls, M. Kist, E. J. Kuipers, and J. G. Kusters. 2002. The role of the ferric uptake regulator (Fur) in regulation of Helicobacter pylori iron uptake. Helicobacter 7:237-244.
40. van Vliet, A. H. M., K. G. Wooldridge, and J. M. Ketley. 1998. Iron-responsive gene regulation in a Campylobacter jejuni fur mutant. J. Bacteriol. 180:5291-5298.
41. Velayudhan, J., N. J. Hughes, A. A. McColm, J. Bagshaw, C. L. Clayton, S. C. Andrews, and D. J. Kelly. 2000. Iron acquisition and virulence in Helicobacter pylori: a major role for FeoB, a high-affinity ferrous iron transporter. Mol. Microbiol. 37:274-286.
42. Wang, S. C., A. V. Dias, and D. B. Zamble. 2009. The "metallo- specific" response of proteins: a perspective based on the Escherichia coli transcriptional regulator NikR. Dalton Trans. 2009:2459-2466.
43. Weinberg, E. D. 2007. Antibiotic properties and applications of lactoferrin. Curr. Pharm. Des. 13:801-811.
44. Whitmire, J. M., H. Gancz, and D. S. Merrell. 2007. Balancing the double-edged sword: metal ion homeostasis and the ulcer bug. Curr. Med. Chem. 14:469-478.
45. Wolfram, L., and P. Bauerfeind. 2009. Activities of urease and nickel uptake of Helicobacter pylori proteins are media- and host-dependent. Helicobacter 14:264-270.
46. Wolfram, L., and P. Bauerfeind. 2002. Conserved low-affinity nickel-binding amino acids are essential for the function of the nickel permease NixA of Helicobacter pylori. J. Bacteriol. 184:1438-1443. (Pubitemid 34157568)
47. 2+ binding selectively promotes binding of Helicobacter pylori NikR to its target urease promoter. J. Mol. Biol. 383:1129-1143.
48. Zhang, Y., D. A. Rodionov, M. S. Gelfand, and V. N. Gladyshev. 2009. Comparative genomic analyses of nickel, cobalt and vitamin B12 utilization. BMC Genomics 10:78.