Potential and Significance of Ammonium Production from Helicobacter pylori

  • KI, Mi-Ran (Graduate School of Biotechnology, Korea University) ;
  • Yun, Soon-Kyu (Graduate School of Biotechnology, Korea University) ;
  • Choi, Kyung-Min (Graduate School of Biotechnology, Korea University) ;
  • Hwang, Se-Young (Graduate School of Biotechnology, Korea University)
  • 발행 : 2003.10.01

초록

Glutamine and urea, abundant in body fluids or plasma, yield net ammonium ions upon hydrolysis by ${\gamma}-glutamyl$ transpeptidase (${\gamma}-GTP$) and urease, respectively, and these two enzymes are largely produced from Helicobacter pylori. To investigate bacterial potential of ammonium production, we first quantified those in whole-cell systems and found that the relative ratio of their amounts varied greatly, especially with pH values and the cell's aging. During the H. pylori cultivation, the ratio appeared to be inversely proportional to each other, showing a progressive increase of the ${\gamma}-GTP$ with decreasing of the urease. Under the urease-defective conditions due to low pH or coccoids, the bacterial cells still possessed a considerable amount of ${\gamma}-GTP$, which was found exclusively in the external compartment, therefore, the cell's ammonium production was found to be solely dependent upon glutamine, and the external ammonium concentration was constant without any contribution of urea concentration. Such ammonium constancy would definitely have an adverse effect on the host, because of its absolute requirement for vacuolar degeneration by H. pylori VacA, maximized at approximately 10 mM $NH_4Cl$. It was also found that, by using the metal-saturated membrane vesicles, ammonium ions were likely to be involved in the pH-dependent cation-flux across the H. pylori membrane, where the role of ${\gamma}-GTP$ in ammonium homeostasis around cells was suggested, especially under the hostile conditions against H. pylori.

키워드

참고문헌

  1. Mol. Microbiol. v.28 Metal ion homeostasis and intracellular parasitism: Microreview Agranoff,D.D.;S.Krishna https://doi.org/10.1046/j.1365-2958.1998.00790.x
  2. Clin. Chim. Acta v.152 Determination of glutamine and glutamate in plasma of men and women by ion exchange chromatography Bos,K.D.;P.Slump https://doi.org/10.1016/0009-8981(85)90193-7
  3. J. Infect. Dis. v.161 Helicobacter pylori and pathogenesis of gastroduodeal inflammation Blaser,M.J. https://doi.org/10.1093/infdis/161.4.626
  4. Mol. Microbiol. v.31 Essential role of Helicobacter pylori γ-glutamyltranspeptidase for the colonization of the gastric mucosa of mice Chevalier,C.;J.M.Thiberge;R.L.Ferrero;A.Labigne https://doi.org/10.1046/j.1365-2958.1999.01271.x
  5. Mol. Cells v.11 Presumptive mechanisms of peptic ulceration by Helicobacter pylori VacA involving mucoprotease and CagA Choi,K.M.;W.J.Lim;J.K.Park;S.Y.Hwang
  6. Infect. Immun. v.63 Helicobacter pylori requires an acidic environment to survive in the presence of urea Clyne,M.;A.Labigne;B.Drumm
  7. AM. J. Surg. Pathol. v.19 Helicobacter pylori and gastric carcinogenesis Corren,P. https://doi.org/10.1097/00000478-199501000-00005
  8. Microbiol. Mol. Biol. Rev. v.63 Helicobacter pylori physiology predicted from genomic comparison of two strains Doig,P.;B.L.de Jonge;R.A.Alm;E.D.Brown;M.Uria-Nickelsen;B.Noonan;S.D.Mills;P.Tummino;G.Carmel;B.C.Guild;D.T.Moir;G.F.Vois;T.J.Trust
  9. Infect. Immun. v.59 Essential role of urease in pathogenesis of gastritis induced by Helicobacter pylori in gnotobiotic piglets Eaton,K.A.;C.L.Brooks;D.R.Morgan;S.Krakowka
  10. Infect. Immun. v.62 Effect of gastric pH on urease-dependent colonization of gnotobiotic piglets by Helicobacter pylori Eaton,K.A.;S.Krakowka
  11. Microb. Ecol. Health Dis. v.4 The importance of urease in acid protection for the gastric colonizing bacteria, Helicobacter pylori and Helicobacter felis Ferrelo,R.L.;A.Lee https://doi.org/10.3109/08910609109140133
  12. J. Microbiol. Biotechnol. v.11 Significance of urease distribution across Helicobacter pylori membrane Gang,J.G.;S.K.Yun;K.M.Choi;W.J.Lim;J.K.Park;S.Y.Hwang
  13. Infect. Immun. v.66 Helicobacter pylori glutamine synthetase lacks features associated with transcriptional and posttranslational regulation Garner,R.M.;J.Fulkerson,Jr.;H.L.T.Mobley
  14. Nature v.388 Cloning and characterization of a mammalian proton-coupled metal-ion transporter Gunshin,H.;B.MacKenzie;U.V.Berger;Y.Gunshin;B.Romero;W.F.Boron;S.Nussberger;J.L.Gollan;M.A.Hediger https://doi.org/10.1038/41343
  15. J. Microbiol. Biotechnol. v.11 Enzyme-linked, biotin-streptavidin bacterial-adhesion assay for Helicobactor pylori lection-like interactions with cultured cells Guzman,M.;Maria-Antonia;F.Ascencio
  16. J. Microbiol. Biotechnol. v.12 Characterization of the nickel resistance gene from Legionella pneumphila: Attenuation of nickel resistance by ppk(polyphosphate kinase) disruption in Escherichia coli Hahm,D.H.;M.J.Yeom;W.M.Ko;E.H.Lee;H.J.Lee;I.Shim;H.Y.Kim
  17. FEMS Microbiol. Lett. v.161 Lack of protection following immunization with H. pylori outer membrane vesicles highlights antigenic differences between H.felis and H.pylori Keenan,J.I.;R.A.Allardyce;P.F.Bagshaw https://doi.org/10.1111/j.1574-6968.1998.tb12924.x
  18. J. Microbiol. Biotechnol. v.9 Effect of omeprazole on membrane P-type ATPase and peptide transport system in Helicobacter pylori Ki,M.R.;S.K.Yun;S.Y.Hwang
  19. J. Med. Microbiol. v.37 Cytopathic effects of Helicobacter pylori on cultured mammalian cells Konishi,H.;M.Ishibashi;M.G.Morshed;T.Nakazawa
  20. Lancet v.2 Unidentified curved bacilli in the stomach of patients with gastritis and peptic ulceration Marshall,B.J.;J.R.Warren
  21. Infect. Immun. v.69 γ-Glutamyltransferase is a Helicobacter pylori virulence factor but is not essential for colonization McGovern,K.J.;T.G.Blanchard;J.A.Gutierrez;S.J.Czinn;S.Krakowka;P.Youngman https://doi.org/10.1128/IAI.69.6.4168-4173.2001
  22. Biochim. Biophys. Acta v.73 γ-Glutamyl-p-nitroanilide: A new convenient substrate for determination and study of L and D-γ-glutamyltranspeptidase activities Orlowski,M.;A.Meister https://doi.org/10.1016/0006-3002(63)90348-2
  23. Trends Microbiol. v.10 The compartment buffered by the urease of Helicobacter pylori: Cytoplasm or periplasm Sachs,G.;D.R.Scott;D.L.Weeks;K.Melchers https://doi.org/10.1016/S0966-842X(02)02346-6
  24. Aliment. Pharmacol. Ther. v.14 Review article: The control of gastric acid and Helicobacter pylori eradication Sachs,G.;J.M.Shin;K.Munson;O.Vagin;N.Lambrecht;D.Scott;D.Weeks;K.Melchers https://doi.org/10.1046/j.1365-2036.2000.00837.x
  25. Gastroenterology v.107 Hydrogen ion concentration in the mucus layer on top of acid-stimulated and -inhibited rat gastric mucosa Schade,C.;G.Flemstrom;L.Holm
  26. J. Biotechnol. v.46 The importance of ammonia in mammalian cell culture Schneider,M.;I.W.Marison;U.von Stockar https://doi.org/10.1016/0168-1656(95)00196-4
  27. Gut v.43 no.Sup. The life and death of Helicobacter pylori Scott,D.;D.Weeks;K.Melchers;G.Sachs https://doi.org/10.1136/gut.43.2008.S56
  28. Gastroenterology v.123 Mechanisms of acid resistance due to the urease system of Helicobacter pylori Scott,D.R.;E.A.Marcus;D.L.Weeks;G.Sachs https://doi.org/10.1053/gast.2002.34218
  29. J. Med. Microbiol. v.44 Factors affecting growth and antibiotic susceptibility of Helicobacter pylori: Effect of pH and urease on the survival of a wild-type strain and a urease-deficient mutant Sjostrom,J.E.;H.Larsson https://doi.org/10.1099/00222615-44-6-425
  30. Digestion v.57 Significance of ammonia in the genesis of gastric epithelial lesions induced by Helicobacter pylori: An in vitro study with different bacterial strains and urea concentrations sommi,P.;V.Ricci,R.;Fiocca,M.;Romano;K.J.Ivey;E.Cova;E.Solcia;U.Ventura https://doi.org/10.1159/000201349
  31. Trends Microbiol. v.10 Acid survival of Helicobacter pylori: How does urease activity trigger cytoplasmic pH homeostasis Stingl,K.;K.Altendorf;E.P.Bakker https://doi.org/10.1016/S0966-842X(01)02287-9
  32. J. Biol. Chem. v.255 The catalytic cycle of gastric ($H^ +\;+\;K^ +$)-ATPase Wallmark,B.;H.B.Stewart;E.Rabon;G.Saccomani;G.Sachs
  33. Anal. Biochem. v.39 Phenol-hypochlorite reaction for determination of ammonia Weatherburn,M.W.
  34. Biochem. Biophys. Res. Commun. v.40 On the reversibility of binding of cardiotonic steroids to a partially purified(Na + K)-activated adenosine triphosphatase from beef brain Yoda,A.;L.E.Hokin https://doi.org/10.1016/0006-291X(70)90985-X
  35. J. Microbiol. Biotechnol. v.7 Characteristics of ATPases present in everted membrane vesicles of Helicobacter pylori Yun,S.K.;S.Y.Hwang
  36. J. Microbiol. Biotechnol. v.10 Cation flux-mediated activation of P-type ATPases in Helicobacter pylori Yun,S.K.;M.R.Ki;J.K.Park;W.J.Lim;S.Y.Hwang