Structure of UreG/UreF/UreH Complex Reveals How Urease Accessory Proteins Facilitate Maturation of Helicobacter pylori Urease

PLoS Biology

Volumn 11, Issue 10, 2013, Pages

  Fong, Yu Hang ^a   Wong, Ho Chun ^a   Yuen, Man Hon ^a   Lau, Pak Ho ^a   Chen, Yu Wai ^b   Wong, Kam Bo ^a  

^a CHINESE UNIVERSITY OF HONG KONG   (Hong Kong)

^b KING'S COLLEGE LONDON   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ALANINE; BACTERIAL PROTEIN; CYSTEINE; DIMER; GUANOSINE TRIPHOSPHATE; HISTIDINE; MONOMER; NICKEL; PROLINE; PROTEIN UREF; PROTEIN UREG; PROTEIN UREH; UNCLASSIFIED DRUG; UREASE;

AMINO ACID SUBSTITUTION; ARTICLE; ATOMIC ABSORPTION SPECTROMETRY; BINDING SITE; CARBAMOYLATION; COMPLEX FORMATION; CONTROLLED STUDY; CRYSTAL STRUCTURE; DIMERIZATION; DISSOCIATION; ENZYME ACTIVATION; HELICOBACTER PYLORI; HYDROLYSIS; IN VITRO STUDY; LIGHT SCATTERING; METAL BINDING; NONHUMAN; PROTEIN ANALYSIS; PROTEIN MOTIF; PROTEIN PROCESSING; PROTEIN STRUCTURE; STRUCTURE ANALYSIS;

HELICOBACTER PYLORI;

BACTERIAL PROTEINS; CRYSTALLOGRAPHY, X-RAY; GUANOSINE TRIPHOSPHATE; HELICOBACTER PYLORI; HYDROLYSIS; IONS; MODELS, MOLECULAR; NICKEL; PROTEIN MULTIMERIZATION; UREASE;

EID: 84886602296     PISSN: 15449173     EISSN: 15457885     Source Type: Journal    
DOI: 10.1371/journal.pbio.1001678     Document Type: Article

References (58)

1. Dupont CL, Yang S, Palenik B, Bourne PE, (2006) Modern proteomes contain putative imprints of ancient shifts in trace metal geochemistry. Proc Natl Acad Sci USA 103: 17822-17827 doi:10.1073/pnas.0605798103.
2. Irving H, Williams RJP, (1948) Order of stability of metal complexes. Nature 162: 746-747 doi:10.1038/162746a0.
3. Lin W, Mathys V, Ang ELY, Koh VHQ, Martínez Gómez JM, et al. (2012) Urease activity represents an alternative pathway for Mycobacterium tuberculosis nitrogen metabolism. Infect Immun 80: 2771-2779 doi:10.1128/IAI.06195-11.
4. Eaton KA, Brooks CL, Morgan DR, Krakowka S, (1991) Essential role of urease in pathogenesis of gastritis induced by Helicobacter pylori in gnotobiotic piglets. Infect Immun 59: 2470-2475.
5. Carter EL, Flugga N, Boer JL, Mulrooney SB, Hausinger RP, (2009) Interplay of metal ions and urease. Metallomics 1: 207-221 doi:10.1039/b903311d.
6. Mulrooney SB, Hausinger RP, (1990) Sequence of the Klebsiella aerogenes urease genes and evidence for accessory proteins facilitating nickel incorporation. J Bacteriol 172: 5837-5843.
7. Labigne A, Cussac V, Courcoux P, (1991) Shuttle cloning and nucleotide sequences of Helicobacter pylori genes responsible for urease activity. J Bacteriol 173: 1920-1931.
8. Park IS, Carr MB, Hausinger RP, (1994) In vitro activation of urease apoprotein and role of UreD as a chaperone required for nickel metallocenter assembly. Proc Natl Acad Sci USA 91: 3233-3237.
9. Moncrief MB, Hausinger RP, (1996) Purification and activation properties of UreD-UreF-urease apoprotein complexes. J Bacteriol 178: 5417-5421.
10. Soriano A, Hausinger RP, (1999) GTP-dependent activation of urease apoprotein in complex with the UreD, UreF, and UreG accessory proteins. Proc Natl Acad Sci USA 96: 11140-11144.
11. Heimer SR, Mobley HL, (2001) Interaction of Proteus mirabilis urease apoenzyme and accessory proteins identified with yeast two-hybrid technology. J Bacteriol 183: 1423-1433 doi:10.1128/JB.183.4.1423-1433.2001.
12. Voland P, Weeks DL, Marcus EA, Prinz C, Sachs G, et al. (2003) Interactions among the seven Helicobacter pylori proteins encoded by the urease gene cluster. Am J Physiol Gastrointest Liver Physiol 284: G96-G106 doi:10.1152/ajpgi.00160.2002.
13. Rain JC, Selig L, De Reuse H, Battaglia V, Reverdy C, et al. (2001) The protein-protein interaction map of Helicobacter pylori. Nature 409: 211-215 doi:10.1038/35051615.
14. Kim JK, Mulrooney SB, Hausinger RP, (2006) The UreEF fusion protein provides a soluble and functional form of the UreF urease accessory protein. J Bacteriol 188: 8413-8420 doi:10.1128/JB.01265-06.
15. Fong YH, Wong HC, Chuck CP, Chen YW, Sun H, et al. (2011) Assembly of preactivation complex for urease maturation in Helicobacter pylori: crystal structure of UreF-UreH protein complex. J Biol Chem 286: 43241-43249 doi:10.1074/jbc.M111.296830.
16. Boer JL, Hausinger RP, (2012) Klebsiella aerogenes UreF: identification of the UreG binding site and role in enhancing the fidelity of urease activation. Biochemistry 51: 2298-2308 doi:10.1021/bi3000897.
17. Leipe DD, Wolf YI, Koonin EV, Aravind L, (2002) Classification and evolution of P-loop GTPases and related ATPases. J Mol Biol 317: 41-72 doi:10.1006/jmbi.2001.5378.
18. Gasper R, Meyer S, Gotthardt K, Sirajuddin M, Wittinghofer A, (2009) It takes two to tango: regulation of G proteins by dimerization. Nat Rev Mol Cell Biol 10: 423-429 doi:10.1038/nrm2689.
19. Mehta N, (2003) Roles of conserved nucleotide-binding domains in accessory proteins, HypB and UreG, in the maturation of nickel-enzymes required for efficient Helicobacter pylori colonization. Microbial Pathogenesis 35: 229-234 doi:10.1016/S0882-4010(03)00151-7.
20. Moncrief MB, Hausinger RP, (1997) Characterization of UreG, identification of a UreD-UreF-UreG complex, and evidence suggesting that a nucleotide-binding site in UreG is required for in vivo metallocenter assembly of Klebsiella aerogenes urease. J Bacteriol 179: 4081-4086.
21. Zambelli B, Turano P, Musiani F, Neyroz P, Ciurli S, (2009) Zn2+-linked dimerization of UreG from Helicobacter pylori, a chaperone involved in nickel trafficking and urease activation. Proteins 74: 222-239 doi:10.1002/prot.22205.
22. Boer JL, Quiroz-Valenzuela S, Anderson KL, Hausinger RP, (2010) Mutagenesis of Klebsiella aerogenes UreG to probe nickel binding and interactions with other urease-related proteins. Biochemistry 49: 5859-5869 doi:10.1021/bi1004987.
23. Shi R, Munger C, Asinas A, Benoit SL, Miller E, et al. (2010) Crystal structures of apo and metal-bound forms of the UreE protein from Helicobacter pylori: role of multiple metal binding sites. Biochemistry 49: 7080-7088 doi:10.1021/bi100372h.
24. Song HK, Mulrooney SB, Huber R, Hausinger RP, (2001) Crystal structure of Klebsiella aerogenes UreE, a nickel-binding metallochaperone for urease activation. J Biol Chem 276: 49359-49364 doi:10.1074/jbc.M108619200.
25. Remaut H, Safarov N, Ciurli S, Van Beeumen J, (2001) Structural basis for Ni(2+) transport and assembly of the urease active site by the metallochaperone UreE from Bacillus pasteurii. J Biol Chem 276: 49365-49370 doi:10.1074/jbc.M108304200.
26. Farrugia MA, Macomber L, Hausinger RP, (2013) Biosynthesis of the urease metallocenter. J Biol Chem 288: 13178-13185 doi:10.1074/jbc.R112.446526.
27. Bellucci M, Zambelli B, Musiani F, Turano P, 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 doi:10.1042/BJ20090434.
28. Park IS, Hausinger RP, (1995) Requirement of carbon dioxide for in vitro assembly of the urease nickel metallocenter. Science 267: 1156-1158.
29. Park IS, Hausinger RP, (1996) Metal ion interaction with urease and UreD-urease apoproteins. Biochemistry 35: 5345-5352 doi:10.1021/bi952894j.
30. Martin-Diaconescu V, Bellucci M, Musiani F, Ciurli S, Maroney MJ, (2012) Unraveling the Helicobacter pylori UreG zinc binding site using X-ray absorption spectroscopy (XAS) and structural modeling. J Biol Inorg Chem 17: 353-361 doi:10.1007/s00775-011-0857-9.
31. Lam R, Romanov V, Johns K, Battaile KP, Wu-Brown J, et al. (2010) Crystal structure of a truncated urease accessory protein UreF from Helicobacter pylori. Proteins 78: 2839-2848 doi:10.1002/prot.22802.
32. Chang Z, Kuchar J, Hausinger RP, (2004) Chemical cross-linking and mass spectrometric identification of sites of interaction for UreD, UreF, and urease. J Biol Chem 279: 15305-15313 doi:10.1074/jbc.M312979200.
33. Quiroz-Valenzuela S, Sukuru SCK, Hausinger RP, Kuhn LA, Heller WT, (2008) The structure of urease activation complexes examined by flexibility analysis, mutagenesis, and small-angle X-ray scattering. Archives of Biochemistry and Biophysics 480: 51-57 doi:10.1016/j.abb.2008.09.004.
34. Vetter IR, (2001) The Guanine Nucleotide-Binding Switch in Three Dimensions. Science 294: 1299-1304 doi:10.1126/science.1062023.
35. Lee MH, Pankratz HS, Wang S, Scott RA, Finnegan MG, et al. (1993) Purification and characterization of Klebsiella aerogenes UreE protein: a nickel-binding protein that functions in urease metallocenter assembly. Protein Sci 2: 1042-1052 doi:10.1002/pro.5560020617.
36. Soriano A, Colpas GJ, Hausinger RP, (2000) UreE stimulation of GTP-dependent urease activation in the UreD-UreF-UreG-urease apoprotein complex. Biochemistry 39: 12435-12440.
37. Benoit S, Maier RJ, (2003) Dependence of Helicobacter pylori urease activity on the nickel-sequestering ability of the UreE accessory protein. J Bacteriol 185: 4787-4795.
38. Banaszak K, Martin-Diaconescu V, Bellucci M, Zambelli B, Rypniewski W, et al. (2012) Crystallographic and X-ray absorption spectroscopic characterization of Helicobacter pylori UreE bound to Ni2+ and Zn2+ reveals a role for the disordered C-terminal arm in metal trafficking. Biochem J 441: 1017-1026 doi:10.1042/BJ20111659.
39. Stingl K, Schauer K, Ecobichon C, Labigne A, Lenormand P, et al. (2008) In vivo interactome of Helicobacter pylori urease revealed by tandem affinity purification. Mol Cell Proteomics 7: 2429-2441 doi:10.1074/mcp.M800160-MCP200.
40. Benoit SL, McMurry JL, Hill SA, Maier RJ, (2012) Helicobacter pylori hydrogenase accessory protein HypA and urease accessory protein UreG compete with each other for UreE recognition. Biochim Biophys Acta 1820: 1519-1525 doi:10.1016/j.bbagen.2012.06.002.
41. Salomone-Stagni M, Zambelli B, Musiani F, Ciurli S, (2007) A model-based proposal for the role of UreF as a GTPase-activating protein in the urease active site biosynthesis. Proteins 68: 749-761 doi:10.1002/prot.21472.
42. Biagi F, Musiani F, Ciurli S, (2013) Structure of the UreD-UreF-UreG-UreE complex in Helicobacter pylori: a model study. J Biol Inorg Chem 18: 571-577 doi:10.1007/s00775-013-1002-8.
43. Scheffzek K, Ahmadian MR, Kabsch W, Wiesmüller L, Lautwein A, et al. (1997) The Ras-RasGAP complex: structural basis for GTPase activation and its loss in oncogenic Ras mutants. Science 277: 333-338 doi:10.1126/science.277.5324.333.
44. Waldron KJ, Robinson NJ, (2009) How do bacterial cells ensure that metalloproteins get the correct metal? Nat Rev Microbiol 7: 25-35 doi:10.1038/nrmicro2057.
45. Chan K-H, Lee K-M, Wong K-B, (2012) Interaction between hydrogenase maturation factors HypA and HypB is required for [NiFe]-hydrogenase maturation. PLoS ONE 7: e32592 doi:10.1371/journal.pone.0032592.
46. Chan K-H, Li T, Wong C-O, Wong K-B, (2012) Structural basis for GTP-dependent dimerization of hydrogenase maturation factor HypB. PLoS ONE 7: e30547 doi:10.1371/journal.pone.0030547.
47. Gasper R, Scrima A, Wittinghofer A, (2006) Structural insights into HypB, a GTP-binding protein that regulates metal binding. J Biol Chem 281: 27492-27502 doi:10.1074/jbc.M600809200.
48. Cai F, Ngu TT, Kaluarachchi H, Zamble DB, (2011) Relationship between the GTPase, metal-binding, and dimerization activities of E. coli HypB. J Biol Inorg Chem 16: 857-868 doi:10.1007/s00775-011-0782-y.
49. Jeoung J-H, Giese T, Grünwald M, Dobbek H, (2009) CooC1 from Carboxydothermus hydrogenoformans is a nickel-binding ATPase. Biochemistry 48: 11505-11513 doi:10.1021/bi901443z.
50. Jeoung J-H, Giese T, Grünwald M, Dobbek H, (2010) Crystal Structure of the ATP-Dependent Maturation Factor of Ni,Fe-Containing Carbon Monoxide Dehydrogenases. J Mol Biol 396: 1165-1179 doi:10.1016/j.jmb.2009.12.062.
51. Kabsch W, (2010) XDS. Acta Crystallogr D Biol Crystallogr 66: 125-132 doi:10.1107/S0907444909047337.
52. McCoy AJ, Grosse-Kunstleve RW, Adams PD, Winn MD, Storoni LC, et al. (2007) Phaser crystallographic software. J Appl Crystallogr 40: 658-674 doi:10.1107/S0021889807021206.
53. Adams PD, Afonine PV, Bunkóczi G, Chen VB, Davis IW, et al. (2010) PHENIX: a comprehensive Python-based system for macromolecular structure solution. Acta Crystallogr D Biol Crystallogr 66: 213-221 doi:10.1107/S0907444909052925.
54. Emsley P, Lohkamp B, Scott WG, Cowtan K, (2010) Features and development of Coot. Acta Crystallogr D Biol Crystallogr 66: 486-501 doi:10.1107/S0907444910007493.
55. Chen VB, Arendall WB, Headd JJ, Keedy DA, Immormino RM, et al. (2010) MolProbity: all-atom structure validation for macromolecular crystallography. Acta Crystallogr D Biol Crystallogr 66: 12-21 doi:10.1107/S0907444909042073.
56. Baykov AA, Evtushenko OA, Avaeva SM, (1988) A malachite green procedure for orthophosphate determination and its use in alkaline phosphatase-based enzyme immunoassay. Anal Biochem 171: 266-270.
57. Weatherburn M, (1967) Phenol-hypochlorite reaction for determination of ammonia. Anal Chem 39: 971-973.
58. Ha NC, Oh ST, Sung JY, Cha KA, Lee MH, et al. (2001) Supramolecular assembly and acid resistance of Helicobacter pylori urease. Nat Struct Biol 8: 505-509 doi:10.1038/88563.