Acid resistance of Helicobacter pylori depends on the UreI membrane protein and an inner membrane proton barrier

Molecular Microbiology

Volumn 36, Issue 1, 2000, Pages 141-152

  Rektorschek, Marina ^a   Buhmann, Anita ^a   Weeks, David ^b   Schwan, Dorothee ^a   Bensch, Klaus W ^a   Eskandari, Sepehr ^b   Scott, David ^b   Sachs, George ^b   Melchers, Klaus ^a  

^a ALTANA PHARMA AG   (Germany)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DETERGENT; MEMBRANE PROTEIN; UREASE;

ARTICLE; BACTERIAL GENETICS; BACTERIAL GROWTH; BACTERIAL MEMBRANE; BACTERIUM MUTANT; ENZYME ACTIVITY; HELICOBACTER PYLORI; OOCYTE; PH; PRIORITY JOURNAL; XENOPUS;

ACIDS; ANIMALS; BACTERIAL PROTEINS; BIOLOGICAL TRANSPORT; CULTURE MEDIA; DRUG RESISTANCE, MICROBIAL; HELICOBACTER PYLORI; HYDROGEN-ION CONCENTRATION; IONOPHORES; MEMBRANE TRANSPORT PROTEINS; MULTIGENE FAMILY; PROTON-MOTIVE FORCE; PROTONS; RECOMBINANT PROTEINS; SALICYLANILIDES; UREA; UREASE; XENOPUS;

BACTERIA (MICROORGANISMS); HELICOBACTER PYLORI; NEGIBACTERIA;

EID: 1642356473     PISSN: 0950382X     EISSN: None     Source Type: Journal    
DOI: 10.1046/j.1365-2958.2000.01835.x     Document Type: Article

References (41)

1. Andrutis, K.A., Fox, J.G., Schauer, D.B., Marini, R.P., Murphy, J.C., Yan, L., et al. (1994) Inability of an isogenic urease-negative mutant strain of Helicobacter mustelae to colonize the ferret stomach. Infect Immun 63: 3722-3725.
2. Ausubel, F.M., Brent, R., Kingston, R.E., Moore, D.D., Seidman, J.G., Smith, J.A., et al. (eds) (1994) Current Protocols in Molecular Biology. New York: John Wiley & Sons.
3. Blazer, M.J. (1992) Hypotheses on the pathogenesis and natural history of Helicobacter pylori-induced inflammation. Gastroenterology 102: 720-727.
4. Borgnia, M.J., Kozono, D., Calamita, G., Maloney, P.C., and Agre, P. (1999) Functional reconstitution and characterization of AqpZ, the E. coli water channel protein. J Mol Biol 29: 11169-11179.
5. Bradford, M. (1976) A rapid and sensitive method for quantification of microgramm quantities of protein, utilizing the principle of protein-dye binding. Anal Biochem 72: 248-252.
6. Chebrou, H., Bigey, F., Arnaud, A., and Galzy, P. (1996) Amide metabolism: a putative ABC transporter in Rhodococcus sp. R312. Gene 182: 215-218.
7. Clyne, M., Labigne, A., and Drumm, B. (1995) Helicobacter pylori requires an acidic environment to survive in the presence of urea. Infect Immun 63 (5): 1669-1673.
8. Cover, T.L., and Blazer, M.J. (1995) Helicobacter pylori: a bacterial cause of gastritis, peptic ulcer disease, and gastric cancer. Am Soc Microb News 61: 21-26.
9. Dunn, B.E., Vakil, N.B., Schneider, B.G., Miller, M.M., Zitzer, J.B., Puetz, T., et al. (1997) Localization of Helicobacter pylori urease and heat shock protein in human gastric biosies. Infect Immun 65: 1181-1188.
10. Eaton, K.A., and Krakowka, S. (1994) Effect of gastric pH on urease-dependent colonization of gnotobiotic piglets by Helicobacter pylori. Infect Immun 62: 3604-3607.
11. Fawcett, J.K., and Scott, J.E. (1960) A rapid and precise method for determination of urea. Clin Pathol 13: 156-159.
12. Ferrero, R.L., Cussac, V., Courcoux, P., and Labigne, A. (1992) Construction of isogenic urease-negative mutants of Helicobacter pylori by allelic exchange. J Bacteriol 174: 4212-4217.
13. Hafeman, D.G., Parce, J.W., and McConnell, H.M. (1988) Light-addressable potentiometric sensor for biochemical systems. Science 240: 1182-1185.
14. Hawtin, P.R., Stacey, A.R., and Newell, D.G. (1990) Investigation of the structure and localization of the urease of Helicobacter pylori using monoclonal antibodies. J Gen Microbiol 136: 1995-2000.
15. Hazell, S.L., and Mendz, G.L. (1997) How Helicobacter pylori works: an overview of the metabolism of Helicobacter pylori. Helicobacter 2: 1-12.
16. Hazell, S.L., Borody, T.J., Gal, A., and Lee, A. (1987) Detection of Campylobacter pylori as a marker of bacterial colonization and gastritis. Infect Immun 66: 4856-4866.
17. Heuermann, D., and Haas, R. (1998) A stable shuttle vector system for efficient genetic complementation of Helicobacter pylori strains by transformation and conjugation. Mol Gen Genet 257: 519-528.
18. Hu, L.-T., and Mobley, H.L.T. (1990) Purification and N-terminal analysis of urease from Helicobacter pylori. Infect Immun 58: 992-998.
19. Karita, M., and Blazer, M. (1998) Acid-tolerance response in Helicobacter pylori and differences between cagA+ and cagA-strains. J Infect Dis 178: 213-219.
20. Krishnamurthy, P., Parlow, Zitzer, J.B., Vakil, N.B., Mobley, H.L.T., Levy, M., Phadnis, S.H., et al. (1998) Helicobacter pylori containing only cytoplasmic urease is susceptible to acid. Infect Immun 66: 5060-5066.
21. McConnell, H.M., Owicki, J.C., Parce, J.W., Miller, D.L., Baxter, G.T., Wada, H.G., et al. (1992) The Cytosensor microphysiometer: biological applications of silicon technology. Science 257: 1906-1912.
22. McGee, D.J., May, C.A., Garner, R.M., Himpsl, J.M., and Mobley, H.L.T. (1999) Isolation of Helicobacter pylori genes that modulate urease activity. J Bacteriol 181: 2477-2484.
23. Meyer-Rosberg, K., Scott, D.R., Rex, D., Melchers, K., and Sachs, G. (1996) The effect of the environmental pH on the proton motive force of Helicobacter pylori. Gastroenterol 111: 886-900.
24. Mobley, H.L.T., Island, M.D., and Hausinger, R.P. (1995) Molecular biology of microbial ureases. Microbiol Rev 59: 451-480.
25. Orbach, E., and Finkelstein, A. (1980) The nonelectrolyte permeability of planar lipid bilayer membranes. J Gen Physiol 75: 427-436.
26. Owicki, J.C., and Parce, J.W. (1992) Biosensors based on the energy metabolism of living cells: the physical chemistry and cell biology of extracellular acidification. Biosen Bioelectr 7: 255-272.
27. Parsonnet, J., Hansen, S., Rodriguez, L., Gelb, A.B., Warnke, A., Jellum, E., et al. (1994) Helicobacter pylori infection and gastric lymphoma. N Engl J Med 330: 1267-1271.
28. Phadnis, S.H., Parlow, M.H., Levy, M., Ilver, D., Caulkins, C.M., Connors, J.B., et al. (1995) Surface localization of Helicobacter pylori urease and a heat shock protein homog requires bacterial autolysis. Infect Immun 64: 905-912.
29. Rektorschek, M., Weeks, D., Sachs, G., and Melchers, K. (1998) The Influence of pH on metabolism and urease activity of Helicobacter pylori. Gastroenterotogy 115: 628-641.
30. Schade, C., Flemstrom, G., and Holm, L. (1994) Hydrogen ion concentration in the mucus layer on top of acid-stimulated and -inhibited rat gastric mucosa. Gastroenterology 107: 180-188.
31. Schägger, H., and Jagow, G. (1987) Tricine-sodium dodecyl sulfate-polyacrylamide gel electrophoresis for the separation of proteins in the range from 1 to 100 kDa. Anal Biochem 166: 368-379.
32. Scott, D.R., Weeks, D., Hong, C., Postius, S., Melchers, K., and Sachs, G. (1998) The role of internal urease in acid resistance of Helicobacter pylori. Gastroenterology 114: 58-70.
33. Shayakul, C., Steel, A., and Hediger, M.A. (1996) Molecular cloning and characterization of the vasopressin-regulated urea transporter of rat kidney collecting ducts. J Clin Invest 98: 2580-2587.
34. Sjöström, J., and Larsson, H. (1996) Factors affecting growth and antibiotic susceptibility of Helicobacter pylori: effect of pH and urea on the survival of a wild-type strain and an urease-deficient mutant. J Med Microbiol 44: 425-433.
35. Skouloubris, S., Thiberge, J.-M., Labigne, A., and De Reuse, H. (1998) The Helicobacter pylori Urel protein is not involved in urease activity but is essential for bacterial survival in vivo. Infect Immun 66: 4517-4521.
36. Tomb, J.F., White, O., Kerlabage, A.R., Clayton, R.A., Sutton, G.G., Fleischmann, R.D., et al. (1997) The complete genome sequence of the gastric pathogen Helicobacter pylori. Nature 388: 539-547.
37. Tsuda, M., Karita, M., Morshed, M.G., Okita, K., and Nakazawa, T.A. (1994) 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.
38. Vanet, A., and Labigne, A. (1998) Evidence for specific secretion rather than autolysis in the release of some Helicobacter pylori proteins. Infect Immun 66: 1023-1027.
39. Warren, J.R., and Marshall, B. (1983) Unidentified curved bacilli on gastric epithelium in active chronic gastritis. Lancet i: 1273-1275.
40. + gated urea channel: The link between Helicobacter pylori urease and gastric colonization. Science 287: 482-485.
41. Wilson, S.A., Williams, R.J., Pearl, L.H., and Drew, R.E. (1995) Identification of two new genes in the Pseudomonas aeruginosa amidase operon, encoding an ATPase (AmiB) and a putative integral membrane protein (AmiS). J Biol Chem 270: 8818-18824.