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PMID: 10572136 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, P.H.S.

Helicobacter pylori rocF is required for arginase activity and acid protection in vitro but is not essential for colonization of mice or for urease activity.

Journal of bacteriology ·Vol. 181 ·No. 23 ·1999-12-00 ·Pages 7314-22

McGee DJ, Radcliff FJ, Mendz GL, Ferrero RL, Mobley HL

Abstract

Arginase of the Helicobacter pylori urea cycle hydrolyzes L-arginine to L-ornithine and urea. H. pylori urease hydrolyzes urea to carbon dioxide and ammonium, which neutralizes acid. Both enzymes are involved in H. pylori nitrogen metabolism. The roles of arginase in the physiology of H. pylori were investigated in vitro and in vivo, since arginase in H. pylori is metabolically upstream of urease and urease is known to be required for colonization of animal models by the bacterium. The H. pylori gene hp1399, which is orthologous to the Bacillus subtilis rocF gene encoding arginase, was cloned, and isogenic allelic exchange mutants of three H. pylori strains were made by using two different constructs: 236-2 and rocF::aphA3. In contrast to wild-type (WT) strains, all rocF mutants were devoid of arginase activity and had diminished serine dehydratase activity, an enzyme activity which generates ammonium. Compared with WT strain 26695 of H. pylori, the rocF::aphA3 mutant was approximately 1, 000-fold more sensitive to acid exposure. The acid sensitivity of the rocF::aphA3 mutant was not reversed by the addition of L-arginine, in contrast to the WT, and yielded a approximately 10, 000-fold difference in viability. Urease activity was similar in both strains and both survived acid exposure equally well when exogenous urea was added, indicating that rocF is not required for urease activity in vitro. Finally, H. pylori mouse-adapted strain SS1 and the 236-2 rocF isogenic mutant colonized mice equally well: 8 of 9 versus 9 of 11 mice, respectively. However, the rocF::aphA3 mutant of strain SS1 had moderately reduced colonization (4 of 10 mice). The geometric mean levels of H. pylori recovered from these mice (in log(10) CFU) were 6.1, 5.5, and 4.1, respectively. Thus, H. pylori rocF is required for arginase activity and is crucial for acid protection in vitro but is not essential for in vivo colonization of mice or for urease activity.

MeSH Terms
Agmatine/metabolism Alleles Animals Arginase/genetics,metabolism Arginine/metabolism Bacterial Proteins Blotting, Southern Cloning, Molecular Deamination Gene Silencing Helicobacter pylori/enzymology,genetics,pathogenicity Hydrogen-Ion Concentration Magnetic Resonance Spectroscopy Mice/microbiology Mutagenesis Urea/pharmacology Urease/metabolism
Chemicals
Bacterial Proteins Agmatine Urea Arginine Urease RocF protein, Helicobacter pylori Arginase
Authors & Affiliations
5 authors, click to expand affiliations / ORCID
McGee D J
Department of Microbiology and Immunology, University of Maryland School of Medicine, Baltimore, Maryland 21201, USA. [email protected]
Radcliff F J
Mendz G L
Ferrero R L
Mobley H L
References (36)
36 references, click to expand
  1. Identification and characterization of an aliphatic amidase in Helicobacter pylori.
    Mol Microbiol. 1997 Sep;25(5):989-98 PMID: 9364923
  2. The complete genome sequence of the gastric pathogen Helicobacter pylori.
    Nature. 1997 Aug 7;388(6642):539-47 PMID: 9252185
  3. Helicobacter pylori containing only cytoplasmic urease is susceptible to acid.
    Infect Immun. 1998 Nov;66(11):5060-6 PMID: 9784504
  4. In situ characterization of Helicobacter pylori arginase.
    Biochim Biophys Acta. 1998 Nov 10;1388(2):465-77 PMID: 9858781
  5. Genomic-sequence comparison of two unrelated isolates of the human gastric pathogen Helicobacter pylori.
    Nature. 1999 Jan 14;397(6715):176-80 PMID: 9923682
  6. Mechanisms of Helicobacter pylori infection: bacterial factors.
    Curr Top Microbiol Immunol. 1999;241:155-80 PMID: 10087661
  7. The tricarboxylic acid cycle of Helicobacter pylori.
    Eur J Biochem. 1999 Feb;260(1):258-67 PMID: 10091606
  8. Isolation of Helicobacter pylori genes that modulate urease activity.
    J Bacteriol. 1999 Apr;181(8):2477-84 PMID: 10198012
  9. Crystal structures of Bacillus caldovelox arginase in complex with substrate and inhibitors reveal new insights into activation, inhibition and catalysis in the arginase superfamily.
    Structure. 1999 Apr 15;7(4):435-48 PMID: 10196128
  10. Unidentified curved bacilli on gastric epithelium in active chronic gastritis.
    Lancet. 1983 Jun 4;1(8336):1273-5 PMID: 6134060
  11. Pyloric Campylobacter infection and gastroduodenal disease.
    Med J Aust. 1985 Apr 15;142(8):439-44 PMID: 3982346
  12. Relation of Campylobacter pyloridis to gastritis and peptic ulcer.
    J Infect Dis. 1986 Apr;153(4):664-9 PMID: 3950448
  13. Gene disruption and replacement as a feasible approach for mutagenesis of Campylobacter jejuni.
    J Bacteriol. 1988 Apr;170(4):1704-8 PMID: 2832375
  14. Helicobacter pylori and the pathogenesis of gastroduodenal inflammation.
    J Infect Dis. 1990 Apr;161(4):626-33 PMID: 2181029
  15. Urea protects Helicobacter (Campylobacter) pylori from the bactericidal effect of acid.
    Gastroenterology. 1990 Sep;99(3):697-702 PMID: 2379775
  16. Shuttle cloning and nucleotide sequences of Helicobacter pylori genes responsible for urease activity.
    J Bacteriol. 1991 Mar;173(6):1920-31 PMID: 2001995
  17. Essential role of urease in pathogenesis of gastritis induced by Helicobacter pylori in gnotobiotic piglets.
    Infect Immun. 1991 Jul;59(7):2470-5 PMID: 2050411
  18. Helicobacter pylori infection and the risk of gastric carcinoma.
    N Engl J Med. 1991 Oct 17;325(16):1127-31 PMID: 1891020
  19. Characterization of Helicobacter pylori urease mutants.
    Infect Immun. 1992 May;60(5):1883-9 PMID: 1563778
  20. Construction of isogenic urease-negative mutants of Helicobacter pylori by allelic exchange.
    J Bacteriol. 1992 Jul;174(13):4212-7 PMID: 1320607
  21. Transformation of Helicobacter pylori by chromosomal metronidazole resistance and by a plasmid with a selectable chloramphenicol resistance marker.
    J Gen Microbiol. 1993 Oct;139(10):2485-93 PMID: 8254319
  22. Effect of gastric pH on urease-dependent colonization of gnotobiotic piglets by Helicobacter pylori.
    Infect Immun. 1994 Sep;62(9):3604-7 PMID: 8063376
  23. Nutritional requirements for growth of Helicobacter pylori.
    Appl Environ Microbiol. 1994 Sep;60(9):3450-3 PMID: 7944377
  24. Analysis in Neisseria meningitidis and other Neisseria species of genes homologous to the FKBP immunophilin family.
    Mol Microbiol. 1993 Oct;10(1):13-23 PMID: 7968509
  25. Pyruvate metabolism in Helicobacter pylori.
    Arch Microbiol. 1994;162(3):187-92 PMID: 7979873
  26. Characteristics of Helicobacter pylori growth in a defined medium and determination of its amino acid requirements.
    Microbiology. 1994 Oct;140 ( Pt 10):2649-56 PMID: 8000535
  27. Helicobacter pylori requires an acidic environment to survive in the presence of urea.
    Infect Immun. 1995 May;63(5):1669-73 PMID: 7729871
  28. Expression of the rocDEF operon involved in arginine catabolism in Bacillus subtilis.
    J Mol Biol. 1995 Jun 23;249(5):843-56 PMID: 7540694
  29. Molecular biology of microbial ureases.
    Microbiol Rev. 1995 Sep;59(3):451-80 PMID: 7565414
  30. Aminoacid utilization by Helicobacter pylori.
    Int J Biochem Cell Biol. 1995 Oct;27(10):1085-93 PMID: 7496998
  31. Factors affecting growth and antibiotic susceptibility of Helicobacter pylori: effect of pH and urea on the survival of a wild-type strain and a urease-deficient mutant.
    J Med Microbiol. 1996 Jun;44(6):425-33 PMID: 8636959
  32. Immunohistochemical study of arginase in cancer of the stomach.
    Virchows Arch. 1996 Aug;428(6):325-31 PMID: 8797936
  33. The urea cycle of Helicobacter pylori.
    Microbiology. 1996 Oct;142 ( Pt 10):2959-67 PMID: 8885413
  34. A standardized mouse model of Helicobacter pylori infection: introducing the Sydney strain.
    Gastroenterology. 1997 Apr;112(4):1386-97 PMID: 9098027
  35. Hyperargininemia presenting as persistent neonatal jaundice and hepatic cirrhosis.
    J Pediatr Gastroenterol Nutr. 1997 Feb;24(2):218-21 PMID: 9106111
  36. Immune responses of specific-pathogen-free mice to chronic Helicobacter pylori (strain SS1) infection.
    Infect Immun. 1998 Apr;66(4):1349-55 PMID: 9529052
Article Info
Journal
Journal of bacteriology
Abbr.
J Bacteriol
ISSN
0021-9193
Published
1999-12-00
Pages
7314-22
Language
English
Region
United States
NLM ID
2985120R
PMCID
PMC103695
Subset
IM
Grants
NIAID NIH HHS · F32 AI010098 · United States
NIAID NIH HHS · R01 AI025567 · United States
NIAID NIH HHS · AI10098 · United States
NIAID NIH HHS · AI25567 · United States
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