Crystal structure of a truncated urease accessory protein UreF from Helicobacter pylori

Proteins: Structure, Function and Bioinformatics

Volumn 78, Issue 13, 2010, Pages 2839-2848

  Lam, Robert ^a   Romanov, Vladimir ^a   Johns, Kathy ^a   Battaile, Kevin P ^b   Wu Brown, Jean ^a   Guthrie, Jennifer L ^a   Hausinger, Robert P ^c,d   Pai, Emil F ^a,e,f   Chirgadze, Nickolay Y ^a,f  

^a PRINCESS MARGARET HOSPITAL   (Canada)

^b ARGONNE NATIONAL LABORATORY   (United States)

^c Michigan State University ^*  (United States)

^d Michigan State University   (United States)

^e UNIVERSITY OF TORONTO   (Canada)

^f UNIVERSITY OF TORONTO   (Canada)

Author keywords

Bacteria; ConSurf; Dimer; Protein protein interactions; Sequence conservation; Urease

Indexed keywords

PROTEIN UREF; UNCLASSIFIED DRUG; UREASE;

ALPHA HELIX; AMINO TERMINAL SEQUENCE; ARTICLE; CARBOXY TERMINAL SEQUENCE; CRYSTAL STRUCTURE; ENZYME BINDING; ENZYME STRUCTURE; GENETIC CONSERVATION; HELICOBACTER PYLORI; NONHUMAN; PRIORITY JOURNAL; PROTEIN FOLDING; PROTEIN SECONDARY STRUCTURE; SEQUENCE ALIGNMENT; STRUCTURE ANALYSIS;

AMINO ACID SEQUENCE; BACTERIAL PROTEINS; BINDING SITES; CRYSTALLOGRAPHY, X-RAY; HELICOBACTER PYLORI; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; MUTATION; PROTEIN FOLDING; PROTEIN MULTIMERIZATION; PROTEIN STRUCTURE, QUATERNARY; PROTEIN STRUCTURE, SECONDARY; SEQUENCE HOMOLOGY, AMINO ACID; UREASE;

HELICOBACTER PYLORI;

EID: 77957945514     PISSN: 08873585     EISSN: 10970134     Source Type: Journal    
DOI: 10.1002/prot.22802     Document Type: Article

References (71)

1. Kusters JG, van Vliet AHM, Kuipers EJ. Pathogenesis of Helicobacter pylori infection. Clin Microbiol Rev 2006;19:449-490.
2. Atherton JC. The pathogenesis of Helicobacter pylori-induced gastro-duodenal diseases. Annu Rev Pathol Mech Dis 2006;1:63-96.
3. Hu L-T, Mobley HLT. Purification and N-terminal analysis of urease from Helicobacter pylori. Infect Immun 1990;58:992-998.
4. Stingl K, Altendorf K, Bakker EP. Acid survival of Helicobacter pylori: how does urease activity trigger cytoplasmic pH homeostasis? Trends Microbiol 2002;10:70-74.
5. Ha N-C, Oh S-T, Sung JY, Cha K-A, Lee MH, Oh B-H. Supramolecular assembly and acid resistance of Helicobacter pylori urease. Nat Struct Biol 2001;8:505-509.
6. Carter EL, Flugga N, Boer JL, Mulrooney SB, Hausinger RP. Interplay of metal ions and urease. Metallomics 2009;1:207-221.
7. Benini S, Rypniewski WR, Wilson KS, Miletti S, Ciurli S, Mangani S. A new proposal for urease mechanism based on the crystal structures of the native and inhibited enzyme from Bacillus pasteurii: why urea hydrolysis costs two nickels. Structure 1999;7:205-216.
8. Jabri E, Carr MB, Hausinger RP, Karplus PA. The crystal structure of urease from Klebsiella aerogenes. Science 1995;268:998-1004.
9. Pearson MA, Michel LO, Hausinger RP, Karplus PA. Structure of Cys319 variants and acetohydroxamate-inhibited Klebsiella aerogenes urease. Biochemistry 1997;36:8164-8172.
10. Sheridan L, Wilmont CM, Cromie KD, van der Logt P, Phillips SEV. Crystallization and preliminary X-ray structure determination of jack bean urease with a bound antibody fragment. Acta Crystallogr D Biol Crystallogr 2002;58:374-376.
11. Maier RJ, Benoit S, Seshadri S. Nickel-binding and accessory proteins facilitating Ni-enzyme maturation in Helicobacter pylori. BioMetals 2007;20:655-664.
12. Cussac V, Ferrero RL, Labigne A. Expression of Helicobacter pylori urease genes in Escherichia coli grown under nitrogen-limiting conditions. J Bacteriol 1992;174:2466-2473.
13. Olson JW, Mehta NS, Maier RJ. Requirement of nickel metabolism proteins HypA and HypB for full activity of both hydrogenase and urease in Helicobacter pylori. Mol Microbiol 2001;39:176-182.
14. Weeks DL, Eskandar S, Scott DR, Sachs G. A H+-gated urea channel: the link between Helicobacter pylori urease and gastric colonization. Science 2000;287:482-485.
15. Benoit S, Maier RJ. Dependence of Helicobacter pylori urease activity on the nickel-sequestering ability of the UreE accessory protein. J Bacteriol 2003;185:4787-4795.
16. Bellucci M, Zambelli B, Musiani F, Turano P, Ciurli S. Helicobacter pylori UreE, a urease accessory protein: specific Ni(2+)and Zn(2+)-binding properties and interaction with its cognate UreG. Biochem J 2009;422:91-100.
17. Mehta N, Benoit S, Maier RJ. Roles of conserved nucleotide-binding domains in accessory proteins, HypB and UreG, in the maturation of nickel-enzymes required for efficient Helicobacter pylori colonization. Microb Pathog 2003;35:229-234.
18. Mehta NS, Olson JW, Maier RJ. Characterization of Helicobacter pylori nickel metabolism accessory proteins needed for maturation of both urease and hydrogenase. J Bacteriol 2003;185:726-734.
19. Benoit SL, Mehta N, Weinberg MV, Maier C, Maier RJ. Interaction between the Helicobacter pylori accessory proteins HypA and UreE is needed for urease maturation. Microbiology 2007;153:1474-1482.
20. Rain J-C, Selig L, de Reuse H, Battaglia V, Reverdy C, Simon S, Lenzen G, Petel F, Wojcik J, Schächter V, Chemama Y, Labigne A, Legrain P. The protein-protein interaction map of Helicobacter pylori. Nature 2001;409:211-215.
21. Voland P, Weeks DL, Marcus EA, Prinz C, Sachs G, Scott D. Interactions among the seven Helicobacter pylori proteins encoded by the urease gene cluster. Am J Physiol Gastrointest Liver Physiol 2003; 284:G96-G106.
22. Moncrief MBC, Hausinger RP. Purification and activation properties of UreD-UreF-urease apoprotein complexes. J Bacteriol 1996; 178:5417-5421.
23. Park I-S, Carr MB, Hausinger RP. In vitro activation of urease apoprotein and role of UreD as a chaperone required for nickel metallocenter assembly. Proc Natl Acad Sci USA 1994;91:3233-3237.
24. Park I-S, Hausinger RP. Evidence for the presence of urease apoprotein complexes containing UreD, UreF, and UreG in cells that are competent for in vivo enzyme activation. J Bacteriol 1995;177: 1947-1951.
25. Moncrief MBC, Hausinger RP. Characterization of UreG, identification of a UreD-UreF-UreG complex, and evidence suggesting that anucleotide-binding site in UreG is required for in vivo metallocenter assembly of Klebsiella aerogenes urease. J Bacteriol 1997;179: 4081-4086.
26. Soriano A, Colpas GJ, Hausinger RP. UreE stimulation of GTP-dependent urease activation in the UreD-UreF-UreG-urease apoprotein complex. Biochemistry 2000;39:12435-12440.
27. Soriano A, Hausinger RP. GTP-dependent activation of urease apoprotein in complex with the UreD, UreF, and UreG accessory proteins. Proc Natl Acad Sci USA 1999;96:11140-11144.
28. Jabri E, Karplus PA. Structures of the Klebsiella aerogenes urease apoprotein and two active-site mutants. Biochemistry 1996;35: 10616-10626.
29. Brayman TG, Hausinger RP. Purification, characterization, and functional analysis of a truncated Klebsiella aerogenes UreE urease accessory protein lacking the histidine-rich carboxyl terminus. J Bacteriol 1996;178:5410-5416.
30. Colpas GJ, Brayman TG, McCracken J, Pressler MA, Babcock GT, Ming L-J, Colangelo CM, Scott RA, Hausinger RP. Spectroscopic characterization of metal binding by Klebsiella aerogenes UreE urease accessory protein. J Biol Inorg Chem 1998;3:150-160.
31. Colpas GJ, Brayman TG, Ming L-J, Hausinger RP. Identification of metal-binding residues in the Klebsiella aerogenes urease nickel metallochaperone, UreE. Biochemistry 1999;38:4078-4088.
32. Grossoehme NE, Mulrooney SB, Hausinger RP, Wilcox DE. Thermodynamics of Ni2+,Cu2+, and Zn2+ binding to urease metallochaperone UreE. Biochemistry 2007;46:10506-10516.
33. Lee MH, Pankratz HS, Wang S, Scott RA, Finnegan MG, Johnson MK, Ippolito JA, Christianson DW, Hausinger RP. Purification and characterization of Klebsiella aerogenes UreE protein: a nickel-binding protein that functions in urease metallocenter assembly. Protein Sci 1993;2:1042-1052.
34. Colpas GJ, Hausinger RP. In vivo and in vitro kinetics of metal transfer by the Klebsiella aerogenes urease nickel metallochaperone, UreE. J Biol Chem 2000;275:10731-10737.
35. Song HK, Mulrooney SB, Huber R, Hausinger RP. Crystal structure of Klebsiella aerogenes UreE, a nickel-binding metallochaperone for urease activation. J Biol Chem 2001;276:49359-49364.
36. Kim JK, Hausinger RP. The UreEF fusion protein provides a soluble and functional form of the UreF urease accessory protein. J Bacteriol 2006;188:8413-8420.
37. Kim KY, Yang CH, Lee MH. Expression of the recombinant Klebsiella aerogenes UreF protein as a MalE fusion. Arch Pharm Res 1999;22:274-278.
38. Sriwanthana B, Island MD, Maneval D, Mobley HLT. Single-step purification of Proteus mirabilis urease accessory protein UreE, a protein with a naturally occurring histidine tail, by nickel chelate affinity chromatography. J Bacteriol 1994;176:6836-6841.
39. Zambelli B, Musiani F, Savini M, Tucker P, Ciurli S. Biochemical studies on Mycobacterium tuberculosis UreG and comparative modeling reveal structural and functional conservation among the bacterial UreG family. Biochemistry 2007;46:3171-3182.
40. Zambelli B, Turano P, Musiani F, Neyroz P, Ciurli S. Zn2+-linked dimerization of UreG from Helicobacter pylori, a chaperone involved in nickel trafficking and urease activation. Proteins 2009;74:222-239.
41. Remaut H, Safarof N, Ciurli S, van Beeumen J. Structural basis for Ni2+ transport and assembly of the urease active site by the metallo-chaperone UreE from Bacillus pasteurii. J Biol Chem 2001;276: 49365-49370.
42. Zambelli B, Stola M, Musiani F, de Vriendt K, Samyn B, Devreese B, van Beeumen J, Dikiy A, Bryant DA, Ciurli S. UreG, a chaperone in the urease assembly process, is an intrinsically unstructured GTPase that specifically binds Zn2+. J Biol Chem 2005;280:4684-4695.
43. Gasper R, Scrima A, Wittinghofer A. Structural insights into HypB, a GTP-binding protein that regulates metal binding. J Biol Chem 2006;281:27492-27502.
44. Otwinowski Z, Minor W. Processing of X-ray diffraction data collected in oscillation mode. Meth Enzymol 1997;276:307-326.
45. Dauter Z, Dauter M, Dodson E. Jolly SAD. Acta Crystallogr D Biol Crystallogr 2002;58:494-506.
46. Dodson E. Is it jolly SAD? Acta Crystallogr D Biol Crystallogr 2003;59:1958-1965.
47. Schneider TR, Sheldrick GM. Substructure solution with SHELXD. Acta Crystallogr D Biol Crystallogr 2002;58:1772-1779.
48. Bricogne G, Vonrhein C, Flensburg C, Schiltz M, Paciorek W. Generation, representation and flow of phase information in structure determination: recent developments in and around SHARP 2.0. Acta Crystallogr D Biol Crystallogr 2003;59:2023-2030.
49. de la Fortelle E, Bricogne G. Maximum-likelihood parameter refinement for multiple isomorphous replacement and multiwavelength anomalous diffraction methods. Meth Enzymol 1997;276:472-494.
50. Perrakis A, Morris R, Lamzin VS. Automated protein model building combined with iterative structure refinement. Nat Struct Biol 1999;6:458-463.
51. Emsley P, Cowtan K. Coot: model-building tools for molecular graphics. Acta Crystallogr D Biol Crystallogr 2004;60:2126-2132.
52. Murshudov GN, Vagin AA, Dodson EJ. Refinement of macromolecular structures by the maximum-likelihood method. Acta Crystallogr D Biol Crystallogr 1997;53:240-255.
53. CCP4. The CCP4 suite: programs for protein crystallography. Acta Crystallogr D Biol Crystallogr 1994;50:760-763.
54. Winn MD, Isupov MN, Murshudov GN. Use of TLS parameters to model anisotropic displacements in macromolecular refinement. Acta Crystallogr D Biol Crystallogr 2001;57:122-133.
55. Winn MD, Murshudov GN, Papiz MZ. Macromolecular TLS refinement in REFMAC at moderate resolutions. Meth Enzymol 2003; 374:300-321.
56. Laskowski RA, MacArthur MW, Moss DS, Thornton JM. PROCHECK: a program to check the stereochemical quality of protein structures. J Appl Crystallogr 1993;26:283-291.
57. DeLano WL. The PYMOL molecular graphic system. San Carlos, CA: DeLano Scientific LLC; 2002.
58. Armon A, Graur D, Ben-Tal N. ConSurf: an algorithmic tool for the identification of functional regions in proteins by surface mapping of phylogenetic information. J Mol Biol 2001;307:447-463.
59. Glaser F, Pupko T, Paz I, Bell RE, Bechor-Shental D, Martz E, Ben- Tal N. ConSurf: identification of functional regions in proteins by surface-mapping of phylogenetic information. Bioinformatics 2003; 19:163-164.
60. Landau M, Mayrose I, Rosenberg Y, Glaser F, Martz E, Pupko T, Ben-Tal N. ConSurf 2005: the projection of evolutionary conservation scores of residues on protein structures. Nucl Acids Res 2005; 33:W299-W302.
61. Cole C, Barber JD, Barton GJ. The Jpred 3 secondary structure prediction server. Nucl Acids Res 2008;36:W197-W201.
62. Chang Z, Kuchar J, Hausinger RP. Chemical crosslinking and mass spectrometric identification of sites of interaction for UreD, UreF, and urease. J Biol Chem 2004;279:15305-15313.
63. Quiroz-Valenzuela S, Sukuru SCK, Hausinger RP, Kuhn LA, Heller WT. The structure of urease activation complexes examined by flexibility analysis, mutagenesis, and small-angle X-ray scattering. Arch Biochem Biophys 2008;480:51-57.
64. Salomone-Stagni M, Zambelli B, Musiani F, Ciurli S. A modelbased proposal for the role of UreF as a GTPase-activating protein in the urease active site biosynthesis. Proteins 2007;68:749-761.
65. Krissinel E, Henrick K. Secondary-structure matching (SSM), a new tool for fast protein structure alignment in three dimensions. Acta Crystallogr D Biol Crystallogr 2004;60:2256-2268.
66. Holm L, Kaariainen S, Rosenstrom P, Schenkel A. Searching protein structure databases with DaliLite v.3. Bioinformatics 2008;24:2780-2781.
67. Pena V, Hothorn M, Eberth A, Kaschau N, Parret A, Gremer L, Bonneau F, Ahmadian MR, Scheffzek K. The C2 domain of Syn- GAP is essential for stimulation of the Rap GTPase reaction. EMBO Rep 2008;9:350-355.
68. Scheffzek K, Ahmadian MR, Wiesmuller L, Kabsch W, Stege P, Schmitz F, Wittinghofer A. Structural analysis of the GAP-related domain from neurofibromin and its implications. EMBO J 1998;17: 4313-4327.
69. Scheffzek K, Lautwein A, Kabsch W, Ahmadian MR, Wittinghofer A. Crystal structure of the GTPase-activating domain of human p120GAP and implications for the interaction with Ras. Nature 1996;384:591-596.
70. Kurella VB, Richard JM, Parke CL, Lecour LF, Jr., Bellamy HD, Worthylake DK. Crystal structure of the GTPase-activating proteinrelated domain from IQGAP1. J Biol Chem 2009;284:14857-14865.
71. Buchwald G, Friebel A, Galan JE, Hardt WD, Wittinghofer A, Scheffzek K. Structural basis for the reversible activation of a Rho protein by the bacterial toxin SopE. EMBO J 2002;21:3286-3295.