Crystal structures of apo and metal-bound forms of the UreE protein from helicobacter pylori: Role of multiple metal binding sites

Biochemistry

Volumn 49, Issue 33, 2010, Pages 7080-7088

  Shi, Rong ^a   Munger, Christine ^a   Asinas, Abdalin ^a   Benoit, Stéphane L ^b   Miller, Erica ^b   Matte, Allan ^c   Maier, Robert J ^b   Cygler, Miroslaw ^a,c  

^a MCGILL UNIVERSITY   (Canada)

^b UNIVERSITY OF GEORGIA   (United States)

^c NATIONAL RESEARCH COUNCIL CANADA   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

CRYSTAL FORMS; HELICOBACTER PYLORI; METAL BINDING; MULTIPLE METALS; N-AND C-TERMINAL DOMAINS; N-TERMINALS; TETRAMERS;

BINDING ENERGY; BINDING SITES; BIOCHEMISTRY; CRYSTAL STRUCTURE; DIMERS; METAL IONS; PROTEINS;

METALS;

HEXAHISTIDINE; HISTIDINE; NICKEL; PROTEIN UREE; UNCLASSIFIED DRUG; UREASE; APOENZYME; BACTERIAL PROTEIN; CARRIER PROTEIN; COPPER; PROTEIN BINDING; UREE PROTEIN, BACTERIA;

AMINO TERMINAL SEQUENCE; ARTICLE; BACTERIAL STRAIN; BINDING SITE; CARBOXY TERMINAL SEQUENCE; CRYSTAL STRUCTURE; HELICOBACTER PYLORI; METAL BINDING; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN STRUCTURE; CHEMICAL STRUCTURE; CHEMISTRY; ENZYMOLOGY; ESCHERICHIA COLI; GENE EXPRESSION; GENETICS; ISOLATION AND PURIFICATION; METABOLISM; PROTEIN CONFORMATION; PROTEIN MULTIMERIZATION; X RAY CRYSTALLOGRAPHY;

APOENZYMES; BACTERIAL PROTEINS; BINDING SITES; CARRIER PROTEINS; COPPER; CRYSTALLOGRAPHY, X-RAY; ESCHERICHIA COLI; GENE EXPRESSION; HELICOBACTER PYLORI; MODELS, MOLECULAR; NICKEL; PROTEIN BINDING; PROTEIN CONFORMATION; PROTEIN MULTIMERIZATION;

HELICOBACTER PYLORI;

EID: 77955689110     PISSN: 00062960     EISSN: 15204995     Source Type: Journal    
DOI: 10.1021/bi100372h     Document Type: Article

References (32)

1. Carter, E. L., Flugga, N., Boer, J. L., Mulrooney, S. B., and Hausinger, R. P. (2009) Interplay of metal ions and urease Metallomics 1, 207-221
2. Mulrooney, S. B. and Hausinger, R. P. (2003) Nickel uptake and utilization by microorganisms FEMS Microbiol. Rev. 27, 239-261
3. Heimer, S. R. and Mobley, H. L. T. (2001) Interaction of proteus mirabilis urease apoenzyme and accessory proteins identified with yeast two-hybrid technology J. Bacteriol. 183, 1423-1433
4. Bellucci, M., Zambelli, B., Musiani, F., Turano, P., and Ciurli, S. (2009) Helicobacter pylori UreE, a urease accessory protein: specific Ni(2+)-and Zn(2+)-binding properties and interaction with its cognate UreG Biochem. J. 422, 91-100
5. Voland, P., Weeks, D. L., Marcus, E. A., Prinz, C., Sachs, G., and Scott, D. (2003) Interactions among the seven Helicobacter pylori proteins encoded by the urease gene cluster Am. J. Physiol. 284, G96-G106
6. Stingl, K., Schauer, K., Ecobichon, C., Labigne, A., Lenormand, P., Rousselle, J. C., Namane, A., and de Reuse, H. (2008) In vivo interactome of Helicobacter pylori urease revealed by tandem affinity purification Mol. Cell. Proteomics 7, 2429-2441
7. Olson, J. W., Mehta, N. S., and Maier, R. J. (2001) Requirement of nickel metabolism proteins HypA and HypB for full activity of both hydrogenase and urease in Helicobacter pylori Mol. Microbiol. 39, 176-182
8. Mehta, N., Olson, J. W., and Maier, R. J. (2003) Characterization of Helicobacter pylori nickel metabolism accessory proteins needed for maturation of both urease and hydrogenase J. Bacteriol. 185, 726-734
9. Benoit, S. L., Zbell, A. L., and Maier, R. J. (2007) Nickel enzyme maturation in Helicobacter hepaticus: roles of accessory proteins in hydrogenase and urease activities Microbiology 153, 3748-3756
10. Lee, M. H., Pankratz, H. S., Wang, S., Scott, R. A., Finnegan, M. G., Johnson, M. K., Ippolito, J. A., Christianson, D. W., and Hausinger, R. P. (1993) Purification and characterization of Klebsiella aerogenes UreE protein: a nickel-binding protein that functions in urease metallocenter assembly Protein Sci. 2, 1042-1052
11. Colpas, G. J., Brayman, T. G., Ming, L. J., and Hausinger, R. P. (1999) Identification of metal-binding residues in the klebsiella aerogenes urease nickel metallochaperone, UreE Biochemistry 38, 4078-4088
12. Soriano, A., Colpas, G. J., and Hausinger, R. P. (2000) UreE stimulation of GTP-dependent urease activation in the UreD-UreF-UreG-urease apoprotein complex Biochemistry 39, 12435-12440
13. Benoit, S. and Maier, R. J. (2003) Dependence of Helicobacter pylori urease activity on the nickel-sequestering ability of the UreE accessory protein J. Bacteriol. 185, 4787-4795
14. 2+ binding to the urease metallochaperone UreE Biochemistry 46, 10506-10516
15. Stola, M., Musiani, F., Mangani, S., Turano, P., Safarov, N., Zambelli, B., and Ciurli, S. (2006) The nickel site of Bacillus pasteurii UreE, a urease metallo-chaperone, as revealed by metal-binding studies and X-ray absorption spectroscopy Biochemistry 45, 6495-6509
16. Musiani, F., Zambelli, B., Stola, M., and Ciurli, S. (2004) Nickel trafficking: insights into the fold and function of UreE, a urease metallochaperone J. Inorg. Biochem. 98, 803-813
17. Ciurli, S., Safarov, N., Miletti, S., Dikiy, A., Christensen, S. K., Kornetzky, K., Bryant, D. A., Vandenberghe, I., Devreese, B., Samyn, B., Remaut, H., and Van Beeumen, J. (2002) Molecular characterization of Bacillus pasteurii UreE, a metal-binding chaperone for the assembly of the urease active site J. Biol. Inorg. Chem. 7, 623-631
18. Song, H. K., Mulrooney, S. B., Huber, R., and Hausinger, R. P. (2001) Crystal structure of Klebsiella aerogenes UreE, a nickel-binding metallochaperone for urease activation J. Biol. Chem. 276, 49359-49364
19. 2+ transport and assembly of the urease active site by the metallochaperone UreE from Bacillus pasteurii J. Biol. Chem. 276, 49365-49370
20. Won, H. S., Lee, Y. H., Kim, J. H., Shin, I. S., Lee, M. H., and Lee, B. J. (2004) Structural characterization of the nickel-binding properties of Bacillus pasteurii urease accessory protein (Ure)E in solution J. Biol. Chem. 279, 17466-17472
21. Ho, S. N., Hunt, H. D., Horton, R. M., Pullen, J. K., and Pease, L. R. (1989) Site-directed mutagenesis by overlap extension using the polymerase chain reaction Gene 77, 51-59
22. Weatherburn, M. W. (1968) Phenol-hypochlorite reaction for determination of ammonia Anal. Chem. 39, 17466-17472
23. Towbin, H., Staehelin, T., and Gordon, J. (1979) Electrophoretic transfer of proteins from polyacrylamide gels to nitrocellulose sheets: procedure and some applications Proc. Natl. Acad. Sci U. S. A. 76, 4350-4354
24. Blake, M. S., Johnston, K. H., Russell-Jones, G. J., and Gotschlich, E. C. (1984) A rapid, sensitive method for detection of alkaline phosphatase-conjugated anti-antibody on Western blots Anal. Biochem. 136, 175-179
25. Benoit, S. L., Mehta, N., Weinberg, M. V., Maier, C., and Maier, R. J. (2007) Interaction between the Helicobacter pylori accessory proteins HypA and UreE is needed for urease maturation Microbiology 153, 1474-1482
26. Otwinowski, Z. and Minor, W. (1997) Processing of X-ray diffraction data collected in oscillation mode Methods Enzymol. 276, 307-326
27. McCoy, A. J., Grosse-Kunstleve, R. W., Adams, P. D., Winn, M. D., Storoni, L. C., and Read, R. J. (2007) Phaser crystallographic software J. Appl. Crystallogr. 40, 658-674
28. Emsley, P. and Cowtan, K. (2004) Coot: model-building tools for molecular graphics Acta Crystallogr. D60, 2126-2132
29. Murshudov, G. N., Vagin, A. A., Lebedev, A., Wilson, K. S., and Dodson, E. J. (1999) Efficient anisotropic refinement of macromolecular structures using FFT Acta Crystallogr. D Biol. Crystallogr. 55, 247-255
30. Brayman, T. G. and Hausinger, R. P. (1996) Purification, characterization, and functional analysis of a truncated Klebsiella aerogenes UreE urease accessory protein lacking the histidine-rich carboxyl terminus J. Bacteriol. 178, 5410-5416
31. Colpas, G. J. and Hausinger, R. P. (2000) In vivo and in vitro kinetics of metal transfer by the Klebsiella aerogenes urease nickel metallochaperone, UreE J. Biol. Chem. 275, 10731-10737
32. Maier, R. J., Benoit, S. L., and Seshadri, S. (2007) Nickel-binding and accessory proteins facilitating Ni-enzyme maturation in Helicobacter pylori Biometals 20, 655-664