Ammonium metabolism enzymes aid Helicobacter pylori acid resistance

Journal of Bacteriology

Volumn 196, Issue 17, 2014, Pages 3074-3081

  Miller, Erica F ^a   Maier, Robert J ^a  

^a UNIVERSITY OF GEORGIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMMONIA; ASPARAGINASE; ASPARAGINE; GLUTAMATE AMMONIA LIGASE; GLUTAMATE DEHYDROGENASE; GLUTAMINASE; GLUTAMINE; NITROGEN; UREA; UREASE;

ACID TOLERANCE; ARTICLE; BACTERIAL STRAIN; CELL LYSATE; COLORIMETRY; DELETION MUTANT; ENZYME METABOLISM; ESCHERICHIA COLI; GENE OVEREXPRESSION; HELICOBACTER PYLORI; LIMIT OF DETECTION; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROMOTER REGION; WILD TYPE;

ACIDS; AMMONIUM COMPOUNDS; ASPARAGINASE; BACTERIAL PROTEINS; GENE EXPRESSION REGULATION, BACTERIAL; GENE EXPRESSION REGULATION, ENZYMOLOGIC; GLUTAMATE DEHYDROGENASE; GLUTAMATE-AMMONIA LIGASE; GLUTAMINASE; HELICOBACTER PYLORI; HYDROGEN-ION CONCENTRATION; PROTON-MOTIVE FORCE; UREASE;

EID: 84905482180     PISSN: 00219193     EISSN: 10985530     Source Type: Journal    
DOI: 10.1128/JB.01423-13     Document Type: Article

References (45)

1. Hu L, Mobley H. 1990. Purification and N-terminal analysis of urease from Helicobacter pylori. Infect. Immun. 58:992-998.
2. Ferrero R, Hazell S, Lee A. 1988. The urease enzymes of Campylobacter pylori and a related bacterium. J. Med. Microbiol. 27:33-40. http://dx.doi.org/10.1099/00222615-27-1-33.
3. Chirica LC, Petersson C, Hurtig M, Jonsson BH, Borén T, Lindskog S. Expression and localization of [alpha]- and [beta]-carbonic anhydrase in Helicobacter pylori. Biochim. Biophys. Acta 1601:192-199. http://dx.doi.org/10.1016/S1570-9639(02)00467-3.
4. Marcus EA, Moshfegh AP, Sachs G, Scott DR. 2005. The periplasmic α-carbonic anhydrase activity of Helicobacter pylori is essential for acid acclimation. J. Bacteriol. 187:729-738. http://dx.doi.org/10.1128/JB.187.2.729-738.2005.
5. Nijevitch AA, Loguinovskaya VV. 2002. Significance of blood urea: gastric ammonia gradient for H. pylori detection in childhood. Dig. Dis. Sci. 47:65-66. (Letter.) http://dx.doi.org/10.1023/A:1013259302767.
6. Neithercut W, Rowe P, El Nujumi A, Dahill S, McColl K. 1993. Effect of Helicobacter pylori infection on intragastric urea and ammonium concentrations in patients with chronic renal failure. J. Clin. Pathol. 46:544-547. http://dx.doi.org/10.1136/jcp.46.6.544.
7. Bury-Moné S, Skouloubris S, Labigne A, De Reuse H. 2001. The Helicobacter pylori UreI protein: role in adaptation to acidity and identification of residues essential for its activity and for acid activation. Mol. Microbiol. 42:1021-1034. http://dx.doi.org/10.1046/j.1365-2958.2001.02689.x.
8. Weeks DL, Eskandari S, Scott DR, Sachs G. 2000. AH+-gated urea channel: the link between Helicobacter pylori urease and gastric colonization. Science 287:482-485. http://dx.doi.org/10.1126/science.287.5452.482.
9. Scott DR, Weeks D, Hong C, Postius S, Melchers K, Sachs G. 1998. The role of internal urease in acid resistance of Helicobacter pylori. Gastroenterology 114:58-70. http://dx.doi.org/10.1016/S0016-5085(98)70633-X.
10. Dunn BE, Campbell GP, Perez-Perez G, Blaser M. 1990. Purification and characterization of urease from Helicobacter pylori. J. Biol. Chem. 265: 9464-9469.
11. Evans DJ, Evans DG, Kirkpatrick SS, Graham DY. 1991. Characterization of the Helicobacter pylori urease and purification of its subunits. Microb. Pathog. 10: 15-26. http://dx.doi.org/10.1016/0882-4010(91)90062-F.
12. Todd MJ, Hausinger RP. 1987. Purification and characterization of the nickel-containing multicomponent urease from Klebsiella aerogenes. J. Biol. Chem. 262: 5963-5967.
13. Clemens DL, Lee BY, Horwitz MA. 1995. Purification, characterization, and genetic analysis of Mycobacterium tuberculosis urease, a potentially critical determinant of host-pathogen interaction. J. Bacteriol. 177: 5644-5652.
14. Breitenbach JM, Hausinger RP. 1988. Proteus mirabilis urease. Partial purification and inhibition by boric acid and boronic acids. Biochem. J. 250: 917-920.
15. Clyne M, Labigne A, Drumm B. 1995. Helicobacter pylori requires an acidic environment to survive in the presence of urea. Infect. Immun. 63:1669-1673.
16. Stingl K, Uhlemann EM, Schmid R, Altendorf K, Bakker EP. 2002. Energetics of Helicobacter pylori and its implications for the mechanism of urease-dependent acid tolerance at pH 1. J. Bacteriol. 184:3053-3060. http://dx.doi.org/10.1128/JB.184.11.3053-3060.2002.
17. Athmann C, Zeng N, Kang T, Marcus EA, Scott DR, Rektorschek M, Buhmann A, Melchers K, Sachs G. 2000. Local pH elevation mediated by the intrabacterial urease of Helicobacter pylori cocultured with gastric cells. J. Clin. Invest. 106:339-347. http://dx.doi.org/10.1172/JCI9351.
18. Meyer-Rosberg K, Scott D, Rex D, Melchers K, Sachs G. 1996. The effect of environmental pH on the proton motive force of Helicobacter pylori. Gastroenterology 111:886-900. http://dx.doi.org/10.1016/S0016-5085 (96)70056-2.
19. Scott DR, Marcus EA, Wen Y, Singh S, Feng J, Sachs G. 2010. Cytoplasmic histidine kinase (HP0244)-regulated assembly of urease withUreI, a channel for urea and its metabolites, CO2, NH3, and NH4+, is necessary for acid survival of Helicobacter pylori. J. Bacteriol. 192:94-103. http://dx.doi.org/10.1128/JB.00848-09.
20. Williams C, Preston T, Hossack M, Slater C, McColl K. 1996. Helicobacter pylori utilises urea for amino acid synthesis. FEMS Immunol. Med. Microbiol. 13:87-94. http://dx.doi.org/10.1111/j.1574-695X.1996.tb00220.x.
21. Garner RM, Fulkerson J, Jr, Mobley HLT. 1998. Helicobacter pylori glutamine synthetase lacks features associated with transcriptional and posttranslational regulation. Infect. Immun. 66:1839-1847.
22. Stingl K, Schauer K, Ecobichon C, Labigne A, Lenormand P, Rousselle JC, Namane A, de Reuse H. 2008. In vivo interactome of Helicobacter pylori urease revealed by tandem affinity purification. Mol. Cell. Proteomics 7:2429-2441. http://dx.doi.org/10.1074/mcp. M800160-MCP200.
23. Kim KM, Lee SG, Park MG, Song JY, Kang HL, Lee WK, Cho MJ, Rhee KH, Youn HS, Baik SC. 2007. [gamma]-Glutamyltranspeptidase of Helicobacter pylori induces mitochondria-mediated apoptosis in AGS cells. Biochem. Biophys. Res. Commun. 355:562-567. http://dx.doi.org/10.1016/j.bbrc.2007.02.021.
24. Scotti C, Sommi P, Pasquetto MV, Cappelletti D, Stivala S, Mignosi P, Savio M, Chiarelli LR, Valentini G, Bolanos-Garcia VM. 2010. Cell-cycle inhibition by Helicobacter pylori L-asparaginase. PLoS One 5:e13892. http://dx.doi.org/10.1371/journal.pone.0013892.
25. Schmees C, Prinz C, Treptau T, Rad R, Hengst L, Voland P, Bauer S, Brenner L, Schmid RM, Gerhard M. 2007. Inhibition of T-cell proliferation by Helicobacter pylori [gamma]-glutamyl transpeptidase. Gastroenterology 132:1820-1833. http://dx.doi.org/10.1053/j.gastro.2007.02.031.
26. Leduc D, Gallaud J, Stingl K, de Reuse H. 2010. Coupled amino acid deamidase-transport systems essential for Helicobacter pylori colonization. Infect. Immun. 78:2782-2792. http://dx.doi.org/10.1128/IAI.00149-10.
27. Benoit S, Maier RJ. 2003. Dependence of Helicobacter pylori urease activity on the nickel-sequestering ability of the UreE accessory protein. J. Bacteriol. 185:4787-4795. http://dx.doi.org/10.1128/JB.185.16.4787-4795.2003.
28. Olson JW, Mehta NS, Maier RJ. 2001. Requirement of nickel metabolism proteins HypA and HypB for full activity of both hydrogenase and urease in Helicobacter pylori. Mol. Microbiol. 39:176-182. http://dx.doi.org/10.1046/j.1365-2958.2001.02244.x.
29. Weatherburn M. 1967. Phenol-hypochlorite reaction for determination of ammonia. Anal. Chem. 39:971-974. http://dx.doi.org/10.1021/ac60252a045.
30. Schmidt E. 1963. Glutamic dehydrogenase, p 752. In Bergmeyer HU (ed), Methods of enzymatic analysis. Academic Press, New York, NY.
31. Bender R, Janssen K, Resnick A, Blumenberg M, Foor F, Magasanik B. Biochemical parameters of glutamine synthetase from Klebsiella aerogenes. J. Bacteriol. 129: 1001-1009.
32. Pahuja SL, Reid TW. 1982. Radioisotope assay for glutamine synthetase using thinlayer chromatography. J. Chromatogr. A 235:249-255. http://dx.doi.org/10.1016/S0021-9673(00)95806-0.
33. Dale T, Court W. 1981. Improved separation of amino acids by thin-layer chromatography. Chromatographia 14:617-620. http://dx.doi.org/10.1007/BF02291097.
34. Stark R, Suleiman MS, Hassan I, Greenman J, Millar M. 1997. Amino acid utilisation and deamidation of glutamine and asparagine by Helicobacter pylori. J. Med. Microbiol. 46:793-800. http://dx.doi.org/10.1099/00222615-46-9-793.
35. Shibayama K, Wachino J, Arakawa Y, Saidijam M, Rutherford NG, Henderson PJF. 2007. Metabolism of glutamine and glutathione via γ-glutamyltranspeptidase and glutamate transport in Helicobacter pylori: possible significance in the pathophysiology of the organism. Mol. Microbiol. 64:396-406. http://dx.doi.org/10.1111/j.1365-2958.2007.05661.x.
36. Shibayama K, Takeuchi H, Wachino J, Mori S, Arakawa Y. 2011. Biochemical and pathophysiological characterization of Helicobacter pylori asparaginase. Microbiol. Immunol. 55:408-417. http://dx.doi.org/10.1111/j.1348-0421.2011.00333.x.
37. Sheppard K, Akochy PM, Salazar JC, Söll D. 2007. The Helicobacter pylori amidotransferase GatCAB is equally efficient in glutaminedependent transamidation of Asp-tRNAAsn and Glu-tRNAGln. J. Biol. Chem. 282:11866-11873. http://dx.doi.org/10.1074/jbc. M700398200.
38. Shapiro BM, Kingdon HS, Stadtman E. 1967. Regulation of glutamine synthetase. VII. Adenylyl glutamine synthetase: a new form of the enzyme with altered regulatory and kinetic properties. Proc. Natl. Acad. Sci. U. S. A. 58: 642-649.
39. Pflock M, Finsterer N, Joseph B, Mollenkopf H, Meyer TF, Beier D. Characterization of the ArsRS regulon of Helicobacter pylori, involved in acid adaptation. J. Bacteriol. 188:3449-3462. http://dx.doi.org/10.1128/JB.188.10.3449-3462.2006.
40. Scott DR, Marcus EA, Wen Y, Oh J, Sachs G. 2007. Gene expression in vivo shows that Helicobacter pylori colonizes an acidic niche on the gastric surface. Proc. Natl. Acad. Sci. U. S. A. 104:7235-7240. http://dx.doi.org/10.1073/pnas.0702300104.
41. Wen Y, Marcus EA, Matrubutham U, Gleeson MA, Scott DR, Sachs G. Acid-adaptive genes of Helicobacter pylori. Infect. Immun. 71: 5921-5939. http://dx.doi.org/10.1128/IAI.71.10.5921-5939.2003.
42. Merrell DS, Goodrich ML, Otto G, Tompkins LS, Falkow S. 2003. pH-regulated gene expression of the gastric pathogen Helicobacter pylori. Infect. Immun. 71: 3529-3539. http://dx.doi.org/10.1128/IAI.71.6.3529-3539.2003.
43. Haüssinger D. 1990. Nitrogen metabolism in liver: structural and functional organization and physiological relevance. Biochem. J. 267: 281-290.
44. Skouloubris S, Thiberge J-M, Labigne A, De Reuse H. 1998. The Helicobacter pylori UreI protein is not involved in urease activity but is essential for bacterial survival in vivo. Infect. Immun. 66: 4517-4521.
45. Kleefeld A, Ackermann B, Bauer J, Krämer J, Unden G. 2009. The fumarate/succinate antiporter DcuB of Escherichia coli is a bifunctional protein with sites for regulation of DcuS-dependent gene expression. J. Biol. Chem. 284: 265-275.