Biosynthesis of active Bacillus subtilis urease in the absence of known urease accessory proteins

Journal of Bacteriology

Volumn 187, Issue 20, 2005, Pages 7150-7154

  Kim, Jong Kyong ^a   Mulrooney, Scott B ^b   Hausinger, Robert P ^a,b,c  

^a MICHIGAN STATE UNIVERSITY   (United States)

^b NONE   (United States)

^c Michigan State University   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GUANOSINE TRIPHOSPHATE; NICKEL; UNCLASSIFIED DRUG; UREASE; UREASE ACCESSORY PROTEIN;

ARTICLE; BACILLUS SUBTILIS; ENZYME ACTIVITY; ENZYME SYNTHESIS; ESCHERICHIA COLI; GENE STRUCTURE; GENETIC RECOMBINATION; IN VIVO STUDY; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; STRUCTURAL GENE;

BACILLUS SUBTILIS; BACTERIAL PROTEINS; ENZYME ACTIVATION; GENE EXPRESSION REGULATION, BACTERIAL; GENE EXPRESSION REGULATION, ENZYMOLOGIC; GUANOSINE TRIPHOSPHATE; HYDROLASES; KLEBSIELLA; NICKEL; RECOMBINANT PROTEINS; UREASE;

BACILLUS SUBTILIS; ESCHERICHIA COLI;

EID: 26444512116     PISSN: 00219193     EISSN: None     Source Type: Journal    
DOI: 10.1128/JB.187.20.7150-7154.2005     Document Type: Article

References (40)

1. Abendroth, J., K. Niefind, O. May, M. Siemann, C. Syldatk, and D. Schomburg. 2002. The structure of L-hydantoinase from Arthrobacter aurescens leads to an understanding of dihydropyrimidinase substrate and enantio specificity. Biochemistry 41:8589-8597.
2. Abendroth, J., K. Niefind, and D. Schomburg. 2002. X-ray structure of a dihydropyrimidinase from Thermus sp. at 1.3 Å resolution. J. Mol. Biol. 320:143-156.
3. Atkinson, M. R., and S. H. Fisher. 1991. Identification of genes and gene products whose expression is activated during nitrogen-limited growth in Bacillus subtilis. J. Bacteriol. 173:23-27.
4. Benini, S., W. R. Rypniewski, K. S. Wilson, S. Miletti, S. Ciurli, and S. Mangani. 1999. A new proposal for urease mechanism based on the crystal structures of the native and inhibited enzme from Bacillus pasteurii: why urea hydrolysis costs two nickels. Structure 7:205-216.
5. Benning, M. M., J. M. Kuo, F. M. Raushel, and H. M. Holden. 1995. Three-dimensional structure of the binuclear metal center of phosphotriesterase. Biochemistry 34:7973-7978.
6. Brayman, T. G., and R. P. Hausinger. 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.
7. Britton, R. A., P. Eichenberger, J. E. Gonzalez-Pastor, P. Fawcett, R. Monson, R. Losick, and A. D. Grossman. 2002. Genome-wide analysis of the stationary-phase sigma factor (sigma-H) regulon of Bacillus subtilis. J. Bacteriol. 184:4881-4890.
8. Chang, Z., J. Kuchar, and R. P. Hausinger. 2004. Chemical crosslinking and mass spectrometric identification of sites of interaction for UreD, UreF, and urease. J. Biol. Chem. 279:15305-15313.
9. Cheon, Y.-H., H.-S. Kim, K.-H. Han, J. Abendroth, K. Niefind, D. Schomburg, J. Wang, and Y. Kim. 2002. Crystal structure of D-hydantoinase from Bacillus stearothennophilus: insight into the stereochemistry of enantioselectivity. Biochemistry 41:9410-9417.
10. Clemens, D. L., B.-Y. Lee, and M. A. Horwitz. 1995. Purification, characterization, and genetic analysis of Mycobacterium tuberculosis urease, a potentially critical determinant of host-pathogen interaction. J. Bacteriol. 177: 5644-5652.
11. Colpas, G. J., and R. P. Hausinger. 2000. In vivo and in vitro kinetics of metal transfer by the Klebsiella aerogenes urease nickel metallochaperone, UreE. J. Biol. Chem. 275:10731-10737.
12. Cruz-Ramos, H., P. Glaser, L. V. Wray, Jr., and S. H. Fisher. 1997. The Bacillus subtilis ureABC operon. J. Bacteriol. 179:3371-3373.
13. Dykxhoorn, D. M., R. St. Pierre, and T. Linn. 1996. A set of compatible tac promoter expression vectors. Gene 177:133-136.
14. Ha, N.-C., S.-T. Oh, J. Y. Sung, K.-A. Cha, M. H. Lee, and B.-H. Oh. 2001. Supramolecular assembly and acid resistance of Helicobacter pylori incase. Nat. Struct. Biol. 8:505-509.
15. Hausinger, R. P., and P. A. Karplus. 2001. Urease, p. 867-879. In K. Wieghardt, R. Huber, T. L. Poulos, and A. Messerschmidt (ed.), Handbook of metalloproteins. John Wiley & Sons, Ltd., West Sussex, United Kingdom.
16. Jahri, E., M. B. Carr, R. P. Hausinger, and P. A. Karplus. 1995. The crystal structure of urease from Klebsiella aerogenes. Science 268:998-1004.
17. Kim, S. D., and R. P. Hausinger. 1994. Genetic organization of the recombinant Bacillus pasteurii urease genes expressed in Escherichia coli. J. Microbiol. Biotechnol. 4:108-112.
18. Kunst, F., N. Ogasawara, I. Moszer, A. M. Alberlini, G. Alloni, V. Azevedo, M. G. Bertero, P. Bessières, A. Bolotin, S. Borchert, R. Borriss, L. Boursier, A. Brans, M. Braun, S. C. Brigneli, S. Bron, S. Brouillet, C. V. Bruschi, B. Caldwell, V. Capuano, N. M. Carter, S.-K. Choi, J.-.I. Codani, I. F. Connerton, N. J. Cummings, R. A. Daniel, F. Denizot, K. M. Devine, A. Düsterhöft, S. D. Ehrlich, P. T. Emmerson, K. D. Entian, J. Errington, C. Fabret, E. Ferrari, D. Foulger, C. Fritz, M. Fujita, Y. Fujita, S. Fuma, A. Galizzi, N. Galleron, S.-Y. Ghim, P. Glaser, A. Goffeau, E. J. Golightly, G. Grandi, G. Guiseppi, B. J. Guy, K. Haga, J. Haiech, C. R. Harwood, A. Hènaut, H. Hubert, S. Holsappel, S. Hosono, M.-F. Hullo, M. Itaya, L. Jones, B. Joris, D. Karamata, Y. Kasahara, M. Klaerr-Blanchard, C. Klein, Y. Kobayashi, P. Koetter, G. Koningstein, S. Krogh, M. Kumano, K. Kurita, A. Lapidus, S. Lardinois, J. Lauber, V. Lazarevic, S.-M. Lee, A. Levine, H. Liu, S. Masuda, C. Mauël, C. Mèdigue, N. Medina, R. P. Mellado, M. Mizuno, D. Moesti, S. Nakai, M. Noback, D. Noone, M. O'Reilly, K. Ogawa, A. Ogiwara, B. Oudega, S.-H. Park, V. Parro, T. M. Pohl, D. Portetelle, S. Porwollik, A. M. Prescott, E. Presecan, P. Pujic, B. Purnelle, et al. 1997. The complete genome sequence of the gram-positive bacterium Bacillus sublilis. Nature 390:249-256.
19. Laemmli, U. K. 1970. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature (London) 227:680-685.
20. Miroux, B., and J. E. Walker. 1996. Over-production of proteins in Escherichia coli: mutant hosts that allow synthesis of some membrane protein and globular proteins at high levels. J. Mol. Biol. 260:289-298.
21. Mizuki, T., M. Kamekura, S. DasSarma, T. Fukushima, T. Usami, Y. Yoshida, and K. Horikoshi. 2004. Ureases of extreme halophiles of the genus Haloarcula with a unique structure of gene cluster. Biosci. Biotechnol. Biochem. 68:397-406.
22. Mobley, H. L. T., M. D. Island, and R. P. Hausinger. 1995. Molecular biology of microbial ureases. Microbiol. Rev. 59:451-480.
23. Mulrooney, S. B., and R. P. Hausinger. 2003. Nickel uptake and utilization by microorganisms. FEMS Microbiol. Rev. 27:239-261.
24. Mulrooney, S. B., and R. P. Hausinger. 1990. Sequence of the Klebsiella aerogenes urease genes and evidence for accessory proteins facilitating niekel incorporation. J. Bacteriol. 172:5837-5843.
25. Mulrooney, S. B., S. K. Ward, and R. P. Hausinger. 2005. Purification and properties of the Klebsiella aerogenes UreE metal-binding domain, a functional metallochaperone of urease. J. Bacteriol. 187:3581-3585.
26. Park, I.-S., and R. P. Hausinger. 1996. Metal ion interactions with urease and UreD-urease apoproteins. Biochemistry 35:5345-5352.
27. Park, I.-S., and R. P. Hausinger. 1995. Requirement of carbon dioxide for in vitro assembly of the urease nickel metallocenter. Science 267:1156-1158.
28. Pearson, M. A., L. O. Michel, R. P. Hausinger, and P. A. Karplus. 1997. Structure of Cys319 variants and acetohydroxamate-inhibited Klebsiella aerogenes urease. Biochemistry 36:8164-8172.
29. Pearson, M. A., I.-S. Park, R. A. Schaller, L. O. Michel, P. A. Karplus, and R. P. Hausinger. 2000. Kinetic and structural characterization of urease active site variants. Biochemistry 39:8575-8584.
30. Sheridan, L., C. M. Wilmont, K. D. Cromie, P. van der Logt, and S. E. V. Phillips. 2001. Crystallization and preliminary X-ray structure determination of jack bean urease with a bound antibody fragment. Acta Crystallogr. D 58:374-376.
31. Soriano, A., G. J. Colpas, and R. P. Hausinger. 2000. UreE stimulation of GTP-dependent urease activation in the UreD-UreF-UreG-urease apoprotein complex. Biochemistry 39:12435-12440.
32. Soriano, A., and R. P. Hausinger. 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.
33. Thoden, J. B., R. Marti-Arbona, F. M. Raushel, and H. M. Holden. 2003. High-resolution x-ray structure of isoaspartyl dipeptidase from Escherichia coli. Biochemistry 42:4874-4882.
34. Thoden, J. B., G. N. Phillips, Jr., T. M. Neal, F. M. Raushel, and H. M. Holden. 2001. Molecular structure of dihydroorotase: a paradigm for catalysis through use of a binuclear metal center. Biochemistry 40:6989-6997.
35. Todd, M. J., and R. P. Hausinger. 1989. Competitive inhibitors of Klebsiella aerogenes urease. Mechanisms of interaction with the nickel active site. J. Biol. Chem. 264:15835-15842.
36. Todd, M. J., and R. P. Hausinger. 1987. Purification and characterization of the nickel-containing muiticomponent urease from Klebsiella aerogenes. J. Biol. Chem. 262:5963-5967.
37. Vasantha, N., and E. Freese. 1980. Enzyme changes during Bacillus subtilis sporulation caused by deprivation of guanine nucleotides. J. Bacteriol. 144: 1119-1125.
38. Weatherburn, M. W. 1967. Phenol-hypochlorite reaction for determination of ammonia. Anal. Chem. 39:971-974.
39. Yamaguchi, K., S. Koshino, F. Akagi, M. Suzuki, A. Uehara, and S. Suzuki. 1997. Structures and catalytic activities of carboxylate-bridged dinickel(II) complexes as models for the metal center of urease. J. Am. Chem. Soc. 119:5752-5753.
40. Zhang, J. W., G. Butland, J. F. Greenblatt, A. Emili, and D. B. Zamble. 2005. A role for SlyD in the Escherichia coli hydrogenase biosynthetic pathway. J. Biol. Chem. 280:4360-4366.