Helicobacter pylori hydrogenase accessory protein HypA and urease accessory protein UreG compete with each other for UreE recognition

Biochimica et Biophysica Acta - General Subjects

Volumn 1820, Issue 10, 2012, Pages 1519-1525

  Benoit, Stéphane L ^a   McMurry, Jonathan L ^b   Hill, Stephanie A ^b   Maier, Robert J ^a  

^a UNIVERSITY OF GEORGIA   (United States)

^b KENNESAW STATE UNIVERSITY   (United States)

Author keywords

Hydrogenase; Metal homeostasis; Metalloenzyme; Nickel; Urease; Zinc

Indexed keywords

BACTERIAL PROTEIN; HYDROGENASE; NICKEL; PROTEIN HYPA; PROTEIN HYPB; PROTEIN UREE; PROTEIN UREG; UNCLASSIFIED DRUG; UREASE; ZINC ION;

ARTICLE; BINDING AFFINITY; BINDING COMPETITION; COMPLEX FORMATION; CONCENTRATION RESPONSE; ENZYME KINETICS; HELICOBACTER PYLORI; IN VITRO STUDY; INTERFEROMETRY; MOLECULAR RECOGNITION; MOLECULAR STABILITY; NONHUMAN; OLIGOMERIZATION; PRIORITY JOURNAL; PROTEIN PROTEIN INTERACTION; SURFACE PLASMON RESONANCE;

BACTERIAL PROTEINS; BINDING SITES; BINDING, COMPETITIVE; CARRIER PROTEINS; GTP-BINDING PROTEINS; HELICOBACTER PYLORI; HYDROGENASE; PROTEIN BINDING; PROTEIN MULTIMERIZATION; SPECTRUM ANALYSIS; SURFACE PLASMON RESONANCE; UREASE;

HELICOBACTER PYLORI;

EID: 84863443663     PISSN: 03044165     EISSN: 18728006     Source Type: Journal    
DOI: 10.1016/j.bbagen.2012.06.002     Document Type: Article

References (35)

1. M.J. Blaser The role of Helicobacter pylori in gastritis and its progression to peptic ulcer disease Aliment. Pharmacol. Ther. 9 Suppl. 1 1995 27 30
2. P. Sipponen, H. Hyvarinen, K. Seppala, and M.J. Blaser Review article: pathogenesis of the transformation from gastritis to malignancy Aliment. Pharmacol. Ther. 12 Suppl. 1 1998 61 71
3. A. Covacci, J.L. Telford, G. Del Giudice, J. Parsonnet, and R. Rappuoli Helicobacter pylori virulence and genetic geography Science 284 1999 1328 1333
4. D.R. Scott, E.A. Marcus, D.L. Weeks, and G. Sachs Mechanisms of acid resistance due to the urease system of Helicobacter pylori Gastroenterology 123 2002 187 195
5. J.W. Olson, and R.J. Maier Molecular hydrogen as an energy source for Helicobacter pylori Science 298 2002 1788 1790
6. V. Cussac, R.L. Ferrero, and A. Labigne Expression of Helicobacter pylori urease genes in Escherichia coli grown under nitrogen-limiting conditions J. Bacteriol. 174 1992 2466 2473
7. E.L. Carter, N. Flugga, J.L. Boer, S.B. Mulrooney, and R.P. Hausinger Interplay of metal ions and urease Metallomics 1 2009 207 221
8. M. Bellucci, B. Zambelli, F. Musiani, P. Turano, and S. Ciurli Helicobacter pylori UreE, a urease accessory protein: specific Ni(2+)- and Zn(2+)-binding properties and interaction with its cognate UreG Biochem. J. 422 2009 91 100
9. S. Benoit, and R.J. Maier Dependence of Helicobacter pylori urease activity on the nickel-sequestering ability of the UreE accessory protein J. Bacteriol. 185 2003 4787 4895
10. R. Shi, C. Munger, A. Asinas, S.L. Benoit, E. Miller, A. Matte, R.J. Maier, and M. Cygler Crystal structures of apo and metal-bound forms of the UreE protein from Helicobacter pylori: role of multiple metal binding sites Biochemistry 49 2010 7080 7088
11. 2+ reveal a role for the disordered C-terminal arm in metal trafficking Biochem. J. 441 2011 1017 1026
12. 2+-linked dimerization of UreG from Helicobacter pylori, a chaperone involved in nickel trafficking and urease activation Proteins 74 2009 222 239
13. N. Mehta, S. Benoit, and R.J. Maier 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. 35 2003 229 234
14. J.W. Olson, N.S. Mehta, and R.J. Maier Requirement of nickel metabolism proteins HypA and HypB for full activity of both hydrogenase and urease in Helicobacter pylori Mol. Microbiol. 39 2001 176 182
15. S.L. Benoit, A.L. Zbell, and R.J. Maier Nickel enzyme maturation in Helicobacter hepaticus: roles of accessory proteins in hydrogenase and urease activities Microbiology 153 2007 3748 3756
16. L. Forzi, and R.G. Sawers Maturation of [NiFe]-hydrogenases in Escherichia coli Biometals 20 2007 565 578
17. H. Kaluarachchi, K.C. Chan Chung, and D.B. Zamble Microbial nickel proteins Nat. Prod. Rep. 27 2010 681 694
18. N. Mehta, J.W. Olson, and R.J. Maier Characterization of Helicobacter pylori nickel metabolism accessory proteins needed for maturation of both urease and hydrogenase J. Bacteriol. 185 2003 726 734
19. R.W. Herbst, I. Perovic, V. Martin-Diaconescu, K. O'Brien, P.T. Chivers, S.S. Pochapsky, T.C. Pochapsky, and M.J. Maroney Communication between the zinc and nickel sites in dimeric HypA: metal recognition and pH sensing J. Am. Chem. Soc. 132 2010 10338 10351
20. W. Xia, H. Li, K.H. Sze, and H. Sun Structure of a nickel chaperone, HypA, from Helicobacter pylori reveals two distinct metal binding sites J. Am. Chem. Soc. 131 2009 10031 10040
21. D.C. Kennedy, R.W. Herbst, J.S. Iwig, P.T. Chivers, and M.J. Maroney A dynamic Zn site in Helicobacter pylori HypA: a potential mechanism for metal-specific protein activity J. Am. Chem. Soc. 129 2007 16 17
22. A.M. Sydor, J. Liu, and D.B. Zamble Effects of metal on the biochemical properties of Helicobacter pylori HypB, a maturation factor of [NiFe]-hydrogenase and urease J. Bacteriol. 193 2011 1359 1368
23. J.C. Rain, L. Selig, H. De Reuse, V. Battaglia, C. Reverdy, S. Simon, G. Lenzen, F. Petel, J. Wojcik, V. Schachter, Y. Chemama, A. Labigne, and P. Legrain The protein-protein interaction map of Helicobacter pylori Nature 409 2001 211 215
24. P. Voland, D.L. Weeks, E.A. Marcus, C. Prinz, G. Sachs, and D. Scott Interactions among the seven Helicobacter pylori proteins encoded by the urease gene cluster Am. J. Physiol. Gastrointest. Liver Physiol. 284 2003 G96 G106
25. K. Stingl, K. Schauer, C. Ecobichon, A. Labigne, P. Lenormand, J.C. Rousselle, A. Namane, and H. de Reuse In vivo interactome of Helicobacter pylori urease revealed by tandem affinity purification Mol. Cell. Proteomics 7 2008 2429 2441
26. W. Xia, H. Li, X. Yang, K.B. Wong, and H. Sun Metallo-GTPase HypB from Helicobacter pylori and its interaction with nickel chaperone protein HypA J. Biol. Chem. 287 2012 6753 6763
27. S.L. Benoit, N. Mehta, M.V. Weinberg, C. Maier, and R.J. Maier Interaction between the Helicobacter pylori accessory proteins HypA and UreE is needed for urease maturation Microbiology 153 2007 1474 1482
28. A. Atanassova, and D.B. Zamble Escherichia coli HypA is a zinc metalloprotein with a weak affinity for nickel J. Bacteriol. 187 2005 4689 4697
29. Y. Abdiche, D. Malashock, A. Pinkerton, and J. Pons Determining kinetics and affinities of protein interactions using a parallel real-time label-free biosensor, the Octet Anal. Biochem. 377 2008 209 217
30. J. Concepcion, K. Witte, C. Wartchow, S. Choo, D. Yao, H. Persson, J. Wei, P. Li, B. Heidecker, W. Ma, R. Varma, L.S. Zhao, D. Perillat, G. Carricato, M. Recknor, K. Du, H. Ho, T. Ellis, J. Gamez, M. Howes, J. Phi-Wilson, S. Lockard, R. Zuk, and H. Tan Label-free detection of biomolecular interactions using BioLayer interferometry for kinetic characterization Comb. Chem. High Throughput Screening 12 2009 791 800
31. J.L. McMurry, C.A. Chrestensen, I.M. Scott, E.W. Lee, A.M. Rahn, A.M. Johansen, B.J. Forsberg, K.D. Harris, and J.C. Salerno Rate, affinity and calcium dependence of nitric oxide synthase isoform binding to the primary physiological regulator calmodulin FEBS J. 278 2011 4943 4954
32. D.P. Morris, E.D. Roush, J.W. Thompson, M.A. Moseley, J.W. Murphy, and J.L. McMurry Kinetic characterization of Salmonella FliK-FlhB interactions demonstrates complexity of the type III secretion substrate-specificity switch Biochemistry 49 2010 6386 6393
33. S. Ciurli, N. Safarov, S. Miletti, A. Dikiy, S.K. Christensen, K. Kornetzky, D.A. Bryant, I. Vandenberghe, B. Devreese, B. Samyn, H. Remaut, and J. van Beeumen Molecular characterization of Bacillus pasteurii UreE, a metal-binding chaperone for the assembly of the urease active site J. Biol. Inorg. Chem. 7 2002 623 631
34. H. Remaut, N. Safarov, S. Ciurli, and J. Van Beeumen Structural basis for Ni(2+) transport and assembly of the urease active site by the metallochaperone UreE from Bacillus pasteurii J. Biol. Chem. 276 2001 49365 49370
35. 2+ binding to the urease metallochaperone UreE Biochemistry 46 2007 10506 10516