Klebsiella aerogenes UreF: Identification of the UreG binding site and role in enhancing the fidelity of urease activation

Biochemistry

Volumn 51, Issue 11, 2012, Pages 2298-2308

  Boer, Jodi L ^a   Hausinger, Robert P ^a,b  

^a Michigan State University   (United States)

^b Michigan State University   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIVE SITE; CELL-FREE EXTRACTS; ENZYME ACTIVATION; FUSION PROTEINS; GTPASE ACTIVITY; GTPASE-ACTIVATING PROTEIN; KLEBSIELLA; PROTEIN-PROTEIN INTERACTIONS; SURFACE RESIDUES; UREASE ACTIVITY; UREASE GENE; WILD TYPES; WILD-TYPE PROTEINS;

CHEMICAL ACTIVATION;

PROTEINS;

APOPROTEIN; GUANOSINE TRIPHOSPHATASE ACTIVATING PROTEIN; METALLOCHAPERONE; UNCLASSIFIED DRUG; UREASE; UREF ENZYME; UREG ENZYME;

ARTICLE; BINDING SITE; CELL FREE SYSTEM; CRYSTAL STRUCTURE; ENZYME ACTIVATION; ENZYME ACTIVITY; ENZYME PURIFICATION; KLEBSIELLA AEROGENES; NONHUMAN; PRIORITY JOURNAL; PROTEIN PROTEIN INTERACTION; SITE DIRECTED MUTAGENESIS;

BACTERIAL PROTEINS; BINDING SITES; ENTEROBACTER AEROGENES; ENZYME ACTIVATION; MULTIGENE FAMILY; MUTAGENESIS, SITE-DIRECTED; UREASE;

KLEBSIELLA AEROGENES;

EID: 84858669770     PISSN: 00062960     EISSN: 15204995     Source Type: Journal    
DOI: 10.1021/bi3000897     Document Type: Article

References (44)

1. Mobley, H. L. T., Island, M. D., and Hausinger, R. P. (1995) Molecular biology of microbial ureases Microbiol. Rev. 59, 451-480
2. Carter, E. L., Flugga, N., Boer, J. L., Mulrooney, S. M., and Hausinger, R. P. (2009) Interplay of metal ions and urease Metallomics 1, 207-221
3. Witte, C.-P. (2011) Urea metabolism in plants Plant Sci. 180, 431-438
4. 2+ in urease: Sensing, trafficking, and catalysis Acc. Chem. Res. 44, 520-530
5. Jabri, E., Carr, M. B., Hausinger, R. P., and Karplus, P. A. (1995) The crystal structure of urease from Klebsiella aerogenes Science 268, 998-1004
6. Lee, M. H., Mulrooney, S. B., and Hausinger, R. P. (1990) Purification, characterization, and in vivo reconstitution of Klebsiella aerogenes urease apoenzyme J. Bacteriol. 172, 4427-4431 (Pubitemid 20236735)
7. Park, I. S., Carr, M. B., and Hausinger, R. P. (1994) In vitro activation of urease apoprotein and role of UreD as a chaperone required for nickel metallocenter assembly Proc. Natl. Acad. Sci. U.S.A. 91, 3233-3237 (Pubitemid 24130210)
8. Moncrief, M. B. C. and Hausinger, R. P. (1996) Purification and activation properties of UreD-UreF-urease apoprotein complexes J. Bacteriol. 178, 5417-5421 (Pubitemid 26304374)
9. Park, I. S. and Hausinger, R. P. (1995) 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. 177, 1947-1951
10. Soriano, A. and Hausinger, R. P. (1999) GTP-dependent activation of urease apoprotein in complex with the UreD, UreF, and UreG accessory proteins Proc. Natl. Acad. Sci. U.S.A. 96, 11140-11144 (Pubitemid 29487347)
11. 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
12. Quiroz-Valenzuela, S., Sukuru, S. C. K., Hausinger, R. P., Kuhn, L. A., and Heller, W. T. (2008) The structure of urease activation complexes examined by flexibility analysis, mutagenesis, and small-angle X-ray scattering Arch. Biochem. Biophys. 480, 51-57
13. Chang, Z. Z., Kuchar, J., and Hausinger, R. P. (2004) Chemical cross-linking and mass spectrometric identification of sites of interaction for UreD, UreF, and urease J. Biol. Chem. 279, 15305-15313 (Pubitemid 38618928)
14. Carter, E. L. and Hausinger, R. P. (2010) Characterization of Klebsiella aerogenes urease accessory protein UreD in fusion with the maltose binding protein J. Bacteriol. 192, 2294-2304
15. Fong, Y. H., Wong, H. C., Chuck, C. P., Chen, Y. W., Sun, H., and Wong, K.-B. (2011) Assembly of preactivation complex for urease maturation in Helicobacter pylori J. Biol. Chem. 286, 43241-43249
16. 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 (Pubitemid 32107739)
17. Rain, J. C., Selig, L., De Reuse, H., Battaglia, V., Reverdy, C., Simon, S., Lenzen, G., Petel, F., Wojcik, J., Schachter, V., Chemama, Y., Labigne, A. S., and Legrain, P. (2001) The protein-protein interaction map of Helicobacter pylori Nature 409, 211-215 (Pubitemid 32144288)
18. Kim, K. Y., Yang, C. H., and Lee, M. H. (1999) Expression of the recombinant Klebsiella aerogenes UreF protein as a MalE fusion Arch. Pharm. Res. 22, 274-278
19. Kim, J. K., Mulrooney, S. B., and Hausinger, R. P. (2006) The UreEF fusion protein provides a soluble and functional form of the UreF urease accessory protein J. Bacteriol. 188, 8413-8420 (Pubitemid 44894041)
20. Lam, R., Romanov, V., Johns, K., Battaile, K. P., Wu-Brown, J., Guthrie, J. L., Hausinger, R. P., Pai, E. F., and Chirgadze, N. Y. (2010) Crystal structure of a truncated urease accessory protein UreF from Helicobacter pylori Proteins 78, 2839-2848
21. Salomone-Stagni, M., Zambelli, B., Musiani, F., and 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 (Pubitemid 47068313)
22. Boer, J. L., Quiroz-Valenzuela, S., Anderson, K. L., and Hausinger, R. P. (2010) Mutagenesis of Klebsiella aerogenes UreG to probe nickel binding and interactions with other urease-related proteins Biochemistry 49, 5859-5869
23. 2+-linked dimerization of UreG from Helicobacter pylori, a chaperone involved in nickel trafficking and urease activation Proteins 74, 222-239
24. 2 J. Biol. Chem. 280, 4684-4695 (Pubitemid 40288638)
25. Zambelli, B., Musiani, F., Savini, M., Tucker, P., and Ciurli, S. (2007) Biochemical studies on Mycobacterium tuberculosis UreG and comparative modeling reveal structural and functional conservation among the bacterial UreG family Biochemistry 46, 3171-3182 (Pubitemid 46449139)
26. 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
27. 2+-binding properties and interaction with its cognate UreG Biochem. J. 422, 91-100
28. Miroux, B. and Walker, J. E. (1996) Over-production of proteins in Escherichia coli: Mutant hosts that allow synthesis of some membrane proteins and globular proteins at high levels J. Mol. Biol. 260, 289-298 (Pubitemid 26254109)
29. Carter, E. L., Boer, J. L., Farrugia, M. A., Flugga, N., Towns, C. L., and Hausinger, R. P. (2011) The function of UreB in Klebsiella aerogenes urease Biochemistry 50, 9296-9308
30. Laemmli, U. K. (1970) Cleavage of structural proteins during assembly of head of bacteriophage-T4 Nature 227, 680
31. Weatherburn, M. W. (1967) Phenol-hypochlorite reaction for determination of ammonia Anal. Chem. 39, 971-974
32. Baykov, A. A., Evtushenko, O. A., and Avaeva, S. M. (1988) A malachite green procedure for orthophosphate determination and its use in alkaline phosphatase-based enzyme immunoassay Anal. Biochem. 171, 266-270
33. Ahmadian, M. R., Stege, P., Scheffzek, K., and Wittinghofer, A. (1997) Confirmation of the arginine-finger hypothesis for the GAP-stimulated GTP-hydrolysis reaction of Ras Nat. Struct. Biol. 4, 686-689
34. Resat, H., Straatsma, T. P., Dixon, D. A., and Miller, J. H. (2001) The arginine finger of RasGAP helps Gln-61 align the nucleophilic water in GAP-stimulated hydrolysis of GTP Proc. Natl. Acad. Sci. U.S.A. 98, 6033-6038 (Pubitemid 32488188)
35. Scheffzek, K. and Ahmadian, M. R. (2005) GTPase activating proteins: Structural and functional insights 18 years after discovery Cell. Mol. Life Sci. 62, 3014-3038 (Pubitemid 43004752)
36. Moncrief, M. B. C. and Hausinger, R. P. (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 (Pubitemid 27291034)
37. Park, I. S. and Hausinger, R. P. (1995) Requirement of carbon-dioxide for in vitro assembly of the urease nickel metallocenter Science 267, 1156-1158
38. Park, I. S. and Hausinger, R. P. (1996) Metal ion interactions with urease and UreD-urease apoproteins Biochemistry 35, 5345-5352 (Pubitemid 26129477)
39. Neyroz, P., Zambelli, B., and Ciurli, S. (2006) Intrinsically disordered structure of Bacillus pasteurii UreG as revealed by steady-state and time-resolved fluorescence spectroscopy Biochemistry 45, 8918-8930 (Pubitemid 44100688)
40. Zambelli, B., Cremades, N., Neyroz, P., Turano, P., Uversky, V. N., and Ciurli, S. (2012) Insights in the (un)structural organization of Bacillus pasteurii UreG, an intrinsically disordered GTPase enzyme Mol. BioSyst. 8, 220-228
41. Chakrabarti, P. P., Suveyzdis, Y., Wittinghofer, A., and Gerwert, K. (2004) Fourier transform infared spectroscopy on the Rap-RapGAP reaction, GTPase activation without an arginine finger J. Biol. Chem. 279, 46226-26233
42. Scrima, A., Thomas, C., Deaconescu, D., and Wittinghofer, A. (2008) The Rap-RapGAP complex: GTP hydrolysis without catalytic glutamine and arginine residues EMBO J. 27, 1145-1153 (Pubitemid 351508140)
43. Kaluarachchi, H., Zhang, J. W., and Zamble, D. B. (2011) Escherichia coli SlyD, more than a Ni(II) reservoir Biochemistry 50, 10761-10763
44. Padovani, D. and Banerjee, R. (2009) A G-protein editor gates coenzyme B-12 loading and is corrupted in methylmalonic aciduria Proc. Natl. Acad. Sci. U.S.A. 106, 21567-21572