A bifunctional urease enhances survival of pathogenic Yersinia enterocolitica and Morganella morganii at low pH

Journal of Bacteriology

Volumn 178, Issue 22, 1996, Pages 6487-6495

  Young, Glenn M ^a   Amid, David ^a   Miller, Virginia L ^a,b  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL ENZYME; UREASE;

ARTICLE; BACTERIAL GROWTH; CELL SURVIVAL; DNA SEQUENCE; ENZYME ACTIVITY; ENZYME ANALYSIS; ENZYME STRUCTURE; HUMAN; MORGANELLA MORGANII; PH; PRIORITY JOURNAL; YERSINIA ENTEROCOLITICA;

BACTERIA (MICROORGANISMS); ESCHERICHIA COLI; HELICOBACTER; KLEBSIELLA PNEUMONIAE; LACTOBACILLUS FERMENTUM; MIRABILIS; MORGANELLA MORGANII; NEGIBACTERIA; PROTEUS MIRABILIS; PROVIDENCIA STUARTII; PSEUDOMONAS; PSEUDOMONAS AERUGINOSA; YERSINIA ENTEROCOLITICA;

EID: 0029952117     PISSN: 00219193     EISSN: None     Source Type: Journal    
DOI: 10.1128/jb.178.22.6487-6495.1996     Document Type: Article

References (49)

1. Blanchard, A. 1990. Ureaplasma urealyticum urease genes: use of a UGA tryptophan codon. Mol. Microbiol. 4:669-678.
2. Brubaker, R. R. 1991. Factor promoting acute and chronic diseases caused by yersiniae. Clin. Microbiol. Rev. 4:309-324.
3. Chen, Y. Y., K. A. Clancy, and R. A. Burne. 1995. Streptococcus salivarius urease: genetic and biochemical characterization and expression in a dental plaque streptococcus. Infect. Immun. 64:585-592.
4. Clemens, D. L., B. Y. Lee, and M. A. Horowitz. 1995. Characterization and genetic analysis of Mycobacterium tuberculosis urease, a potentially critical determinant of host-pathogen interaction. J. Bacteriol. 177:5644-5652.
5. Clyne, M., A. Labigne, and B. Drumm. 1995. Helicobacter pylori requires an acidic environment to survive in the presence of urea. Infect. Immun. 63:1669-1673.
6. Collins, C., and S. Falkow. 1990. Genetic analysis of Escherichia coli urease genes: evidence for two distinct loci. J. Bacteriol. 172:7138-7144.
7. Collins, C. M., D. M. Gutman, and H. Laman. 1993. Identification of a nitrogen-regulated promoter controlling expression of Klebsiella pneumoniae urease genes. Mol. Microbiol. 8:187-198.
8. Cornelis, G., Y. Laroche, G. Balligand, M.-P. Sory, and G. Wauters. 1987. Yersinia enterocolitica, a primary model for bacterial invasiveness. Rev. Infect. Dis. 9:64-87.
9. de Koning-Ward, T. F., A. C. Ward, and R. M. Robins-Browne. 1994. Characterization of the urease-encoding gene complex of Yersinia enterocolitica. Gene 145:25-32
10. de Koning-Ward, T. F., and R. M. Robins-Browne. 1995. Contribution of urease to acid tolerance in Yersinia enterocolitica. Infect. Immun. 63:3790-3795.
11. Dunn, B. E., G. P. Campbell, G. I. Perez-Perez, and M. J. Blaser. 1990. Purification and characterization of urease of Helicobacter pylori. J. Biol. Chem. 265:9464-9469.
12. Eaton, K. A., C. L. Brooks, D. R. Morgan, and S. Krakowka. 1991. Essential role of urease in pathogenesis of gastritis induced by Helicobacter pylori in gnotobiotic piglets. Infect. Immun. 59:2470-2475.
13. Evans, D. J., D. G. Evans, S. S. Kirkpatrick, and D. Y. Graham. 1991 Characterization of the Helicobacter pylori urease and purification of its subunits. Microb. Pathog. 10:15-26.
14. Ferrero, R. L., and A. Labigne. 1993. Cloning, expression and sequencing of Helicobacter felis urease genes. Mol. Microbiol. 9:323-333.
15. Fleischmann, R. D., M. D. Adams, O. While, R. A. Clayton, E. F. Kirkness, A. R. Kerlavage, C. J. Bult, J.-F. Tomb, B. A. Dougherty, J. M. Merrick, K. McKenney, G. Sutton, W. FitzHugh, C. Fields, J. D. Gocayne, J. Scott, R. Shirley, L.-I. Liu, A. Glodek, J. M. Kelley, J. F. Weidman, C. A. Phillips, T. Springs, E. Hedblom, M. D. Cotton, T. R. Utterback, M. C. Hanna, D. T. Nguyen, D. M. Saudek, R. C. Brandon, L. D. Fine, J. L. Fritchman, J. L. Fuhrmann, N. S. M. Geoghagen, C. L. Gnehm, L. A. McDonald, K. V. Small, C. M. Fraser, H. O. Smith, and J. C. Venter. 1995. Whole-genome random sequencing and assembly of Haemophilus influenzae Rd. Science 269:496-512.
16. Giannella, R. A., S. A. Broitman, and N. Zamcheck. 1972. Gastric acid barrier to ingested microorganisms in man: studies in vivo and in vitro. Gut 13:251-256.
17. Hawtin, P. R., A. R. Stacey, and D. G. Newell. 1991. Investigation of the structure and localization of the urease of Helicobacter pylori using monoclonal antibodies. J. Gen. Microbiol. 136:1995-2000.
18. Hu, L.-T., E. B. Nicholson, B. D. Jones, M. J. Lynch, and H. L. T. Mobley. 1990. Morganella morganii urease: purification, characterization, and isolation of gene sequences. J. Bacteriol. 172:3073-3080.
19. Jabri, E., M. B. Carr, R. P. Hausinger, and P. A. Karplus. 1995. The crystal structure of urease from Klebsiella aerogenes. Science 268:998-1004.
20. Jones, B. D., and H. T. L. Mobley. 1989. Proteus mirabilis urease: nucleotide sequence determination and comparison with jack bean urease. J. Bacteriol. 171:6414-6422.
21. Jose, J., U. K. Schafer, and H. Kaltwasser. 1994. Threonine is present instead of cysteine at the active site of urease from Staphylococcus xylosus. Arch. Microbiol. 161:384-392.
22. Kinder, S. A., J. L. Badger, G. O. Bryant, J. C. Pepe, and V. L. Miller. 1993. Cloning the YenI endonuclease and methyltransferase from Yersinia enterocolitica serotype O:8 and construction of a transformable R-M+ mutant. Gene 136:271-275.
23. Labigne, A., V. Cussac, and P. Couroux. 1991. Shuttle cloning and nucleotide sequences of Helicobacter pylori genes responsible for urease activity. J. Bacteriol. 173:1920-1931.
24. Maeda, M., M. Hidaka, A. Nakamura, H. Masaki, and T. Uozumi. 1994. Cloning, sequencing, and expression of thermophilic Bacillus sp. strain TB-90 urease gene complex in Escherichia coli. J. Bacteriol. 176:432-442.
25. Mahan, M. J., J. W. Tonbias, J. M. Slauch, P. C. Hanna, R. J. Collier, and J. J. Mekalanos. 1995. Antibiotic-based selection for bacterial genes that are specifically induced during infection of a host. Proc. Natl. Acad. Sci. USA 92:669-673.
26. Marshall, B. J., L. J. Barrett, C. Prakash, R. W. McCallum, and R. L. Guerrant. 1990. Urea protects Helicobacter (Campylobacter) pylori from the bactericidal effect of acid. Gastroenterology 99:697-702.
27. Miksch, G., W. Arnold, P. Lentzsch, U. B. Preifer, and A. Puhler. 1994. A 4.6 kb DNA region of Rhizobium meliloti involved in determining urease and hydrogenase activities carries the structural genes for urease (ureA, ureB, ureC) interrupted by other open reading frames. Mol. Gen. Genet. 242:539-550.
28. Miller, J. H. 1972. Experiments in molecular genetics. Cold Spring Harbor Laboratory, Cold Spring Harbor, N.Y.
29. Mobley, H. L. T., M. J. Cortesia, L. E. Rosenthal, and B. D. Jones. 1988. Characterization of urease from Campylobacter pylori. J. Clin. Microbiol. 26:831-836.
30. Mobley, H. L. T., and R. P. Hausinger. 1989. Microbial ureases: significance, regulation, and molecular characterization. Microbiol. Rev. 53:85-108.
31. Mobley, H. L. T., R. E. Garner, and P. Bauerfeind. 1995. Helicobacter pylori nickel dependent transport gene nixA: synthesis of catalytically active urease in E. coli independent of growth conditions. Mol. Microbiol. 16:97-109.
32. Mobley, H. L. T., M. D. Island, and R. Hausinger. 1995. Molecular biology of microbial ureases. Microbiol. Rev. 59:451-480.
33. Morsdorf, G. P., and H. Kaltwasser. 1989. Cloning of the genes encoding urease from Proteus vulgaris and sequencing of the structural genes. FEMS Microbiol. Lett. 66:67-74.
34. Morsdorf, G., P. Weinmann, and H. Kaltwasser. 1994. Nucleotide sequence of the three genes on a urease encoding DNA-fragment from Bacillus pasteurii. GenBank accession number X78411.
35. Mulrooney, S. B., and R. P. Hausinger. 1990. Sequence of the Klebsiella aerogenes urease genes and evidence for accessory proteins facilitating nickel incorporation. J. Bacteriol. 172:5837-5843.
36. Pepe, J. C., and V. L. Miller. 1993. Yersinia enterocolitica invasin: a primary role in the initiation of infection. Proc. Natl. Acad. Sci. USA 90:6473-6477.
37. Perez-Perez, G. I., A. Z. Olivares, T. L. Cover, and M. J. Blaser. 1992. Characterization of Helicobacter pylori variants selected for urease deficiency. Infect. Immun. 60:3658-3663.
38. Phadnis, S. H., M. H. Parlow, M. Levy, D. Ilver, C. M. Caulkins, J. B. Connors, and B. E. Dunn. 1996. Surface localization of Helicobacter pylori urease and a heat shock protein homolog requires bacterial autolysis. Infect. Immun. 64:905-912.
39. Prentki, P., and H. M. Krinsch. 1984. In vivo insertion mutagenesis with a selectable DNA fragment. Gene 29:303-313.
40. Sanger, F., S. Nicklen, and A. R. Coulson. 1977. DNA sequencing using chain-terminating inhibitors. Proc. Natl. Acad. Sci. USA 74:5463-5467.
41. Simon, R., U. Priefer, and A. Puhler. 1983. A broad host range mobilization system for in vivo genetic engineering: transposon mutagenesis in Gram negative bacteria. Bio/Technology 1:784-791.
42. Smith, G. R., Y. S. Halpern, and B. Magasanik. 1971 Genetic and metabolic control of enzymes responsible for histidine degradation in Salmonella typhimurium. J. Biol. Chem. 246:3320-3329.
43. Southern, E. M. 1975. Detection of specific sequences among DNA fragments separated by gel electrophoresis. J. Mol. Biol. 98:503-517.
44. Suzuki, K., V. Benno, T. Mitsuoka, S. Takebe, K. Kobashi, and J. Hase. 1979. Urease-producing species of the intestinal anaerobes and their activities. Appl. Environ. Microbiol. 37:379-382.
45. Suzuki, K., M. Takahashi, S. Imamura, and T. Ishikawa. 1992. Nucleotide sequence of acid urease of Lactobacillus fermentum JCM5869. GenBank accession number D10605.
46. Takahashi, S., H. Igarashi, K. Nakamura, N. Masubuchi, S. Saito, T. Aoyagi, T. Itoh, and I. Hirata. 1993. Helicobacter pylori urease activity - comparative study between urease positive and urease negative strains. Jpn. J. Clin. Med. 51:3149-3153.
47. Takishima, K., T. Suga, and G. Mamiya. 1988. The structure of jack bean urease. The complete amino acid sequence, limited proteolysis and reactive cysteine residues. Eur. J. Biochem. 175:151-165.
48. Tsuda, M., M. Karita, M. G. Morshed, K. Okita, and T. Nakasaki. 1994. A urease-negative mutant of Helicobacter pylori constructed by allelic exchange mutagenesis lacks the ability to colonize the nude mouse stomach. Infect. Immun. 62:3586-3589.
49. Wolfram, L., B. Friedrich, and T. Eitinger. 1995. The Alcaligenes eutrophus protein HoxN mediates nickel transport in Escherichia coli. J. Bacteriol. 177:1840-1843.