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PMID: 14500481 Published · ppublish English Comparative Study Journal Article Research Support, U.S. Gov't, P.H.S.

Presence of active aliphatic amidases in Helicobacter species able to colonize the stomach.

Infection and immunity ·Vol. 71 ·No. 10 ·2003-10-00 ·Pages 5613-22

Bury-Moné S, Skouloubris S, Dauga C, Thiberge JM, Dailidiene D, Berg DE, Labigne A, De Reuse H

Abstract

Ammonia production is of great importance for the gastric pathogen Helicobacter pylori as a nitrogen source, as a compound protecting against gastric acidity, and as a cytotoxic molecule. In addition to urease, H. pylori possesses two aliphatic amidases responsible for ammonia production: AmiE, a classical amidase, and AmiF, a new type of formamidase. Both enzymes are part of a regulatory network consisting of nitrogen metabolism enzymes, including urease and arginase. We examined the role of the H. pylori amidases in vivo by testing the gastric colonization of mice with H. pylori SS1 strains carrying mutations in amiE and/or amiF and in coinfection experiments with wild-type and double mutant strains. A new cassette conferring resistance to gentamicin was used in addition to the kanamycin cassette to construct the double mutation in strain SS1. Our data indicate that the amidases are not essential for colonization of mice. The search for amiE and amiF genes in 53 H. pylori strains from different geographic origins indicated the presence of both genes in all these genomes. We tested for the presence of the amiE and amiF genes and for amidase and formamidase activities in eleven Helicobacter species. Among the gastric species, H. acinonychis possessed both amiE and amiF, H. felis carried only amiF, and H. mustelae was devoid of amidases. H. muridarum, which can colonize both mouse intestine and stomach, was the only enterohepatic species to contain amiE. Phylogenetic trees based upon the sequences of H. pylori amiE and amiF genes and their respective homologs from other organisms as well as the amidase gene distribution among Helicobacter species are strongly suggestive of amidase acquisition by horizontal gene transfer. Since amidases are found only in Helicobacter species able to colonize the stomach, their acquisition might be related to selective pressure in this particular gastric environment.

MeSH Terms
Amidohydrolases/genetics,metabolism Animals Base Sequence DNA, Bacterial/genetics Drug Resistance, Bacterial/genetics Female Genes, Bacterial Helicobacter/enzymology,genetics,pathogenicity Helicobacter pylori/enzymology,genetics,pathogenicity Humans Mice Mutagenesis, Insertional Mutation Phylogeny Species Specificity Stomach/microbiology Virulence/genetics,physiology
Chemicals
DNA, Bacterial Amidohydrolases amidase formamidase
Authors & Affiliations
8 authors, click to expand affiliations / ORCID
Bury-Moné Stéphanie
Unité de Pathogénie Bactérienne des Muqueuses, Département de Pathogenèse Microbienne. Département Structure et Dynamique des Génomes, Institut Pasteur, 28 Rue du Docteur Roux, 75724 Paris Cedex 15, France.
Skouloubris Stéphane
Dauga Catherine
Thiberge Jean-Michel
Dailidiene Daiva
Berg Douglas E
Labigne Agnès
De Reuse Hilde
References (47)
47 references, click to expand
  1. Essential role of Helicobacter pylori gamma-glutamyltranspeptidase for the colonization of the gastric mucosa of mice.
    Mol Microbiol. 1999 Mar;31(5):1359-72 PMID: 10200957
  2. Phenotypic changes of Helicobacter pylori components during an experimental infection in mice.
    FEMS Immunol Med Microbiol. 1999 May;24(1):27-33 PMID: 10340709
  3. Sequence variation in Helicobacter pylori.
    Trends Microbiol. 2000 Feb;8(2):57-8 PMID: 10664596
  4. The disease spectrum of Helicobacter pylori: the immunopathogenesis of gastroduodenal ulcer and gastric cancer.
    Annu Rev Microbiol. 2000;54:615-40 PMID: 11018139
  5. Emergence of diverse Helicobacter species in the pathogenesis of gastric and enterohepatic diseases.
    Clin Microbiol Rev. 2001 Jan;14(1):59-97 PMID: 11148003
  6. Vacuolating cytotoxin of Helicobacter pylori plays a role during colonization in a mouse model of infection.
    Infect Immun. 2001 Feb;69(2):730-6 PMID: 11159961
  7. Ammonia as an accelerator of tumor necrosis factor alpha-induced apoptosis of gastric epithelial cells in Helicobacter pylori infection.
    Infect Immun. 2001 Feb;69(2):816-21 PMID: 11159973
  8. afa-8 Gene cluster is carried by a pathogenicity island inserted into the tRNA(Phe) of human and bovine pathogenic Escherichia coli isolates.
    Infect Immun. 2001 Feb;69(2):937-48 PMID: 11159989
  9. Effects of Helicobacter pylori infection on gastric acid secretion and serum gastrin levels in Mongolian gerbils.
    Gut. 2001 Jun;48(6):765-73 PMID: 11358893
  10. The AmiE aliphatic amidase and AmiF formamidase of Helicobacter pylori: natural evolution of two enzyme paralogues.
    Mol Microbiol. 2001 May;40(3):596-609 PMID: 11359566
  11. Selecting models of nucleotide substitution: an application to human immunodeficiency virus 1 (HIV-1).
    Mol Biol Evol. 2001 Jun;18(6):897-906 PMID: 11371577
  12. Pathogenicity islands: the tip of the iceberg.
    Microbes Infect. 2001 Jun;3(7):545-8 PMID: 11418328
  13. The Helicobacter pylori UreI protein: role in adaptation to acidity and identification of residues essential for its activity and for acid activation.
    Mol Microbiol. 2001 Nov;42(4):1021-34 PMID: 11737644
  14. Reconciling the many faces of lateral gene transfer.
    Trends Microbiol. 2002 Jan;10(1):1-4 PMID: 11755071
  15. Immunoproteomics of Helicobacter pylori infection and relation to gastric disease.
    Proteomics. 2002 Mar;2(3):313-24 PMID: 11921447
  16. A phylogenomic approach to bacterial phylogeny: evidence of a core of genes sharing a common history.
    Genome Res. 2002 Jul;12(7):1080-90 PMID: 12097345
  17. The complete genome sequence of the carcinogenic bacterium Helicobacter hepaticus.
    Proc Natl Acad Sci U S A. 2003 Jun 24;100(13):7901-6 PMID: 12810954
  18. Construction of isogenic urease-negative mutants of Helicobacter pylori by allelic exchange.
    J Bacteriol. 1992 Jul;174(13):4212-7 PMID: 1320607
  19. Phylogeny of Helicobacter felis sp. nov., Helicobacter mustelae, and related bacteria.
    Int J Syst Bacteriol. 1991 Jan;41(1):31-8 PMID: 1704791
  20. Revision of Campylobacter, Helicobacter, and Wolinella taxonomy: emendation of generic descriptions and proposal of Arcobacter gen. nov.
    Int J Syst Bacteriol. 1991 Jan;41(1):88-103 PMID: 1704793
  21. Helicobacter muridarum sp. nov., a microaerophilic helical bacterium with a novel ultrastructure isolated from the intestinal mucosa of rodents.
    Int J Syst Bacteriol. 1992 Jan;42(1):27-36 PMID: 1736969
  22. Shuttle cloning and nucleotide sequences of Helicobacter pylori genes responsible for urease activity.
    J Bacteriol. 1991 Mar;173(6):1920-31 PMID: 2001995
  23. The general stochastic model of nucleotide substitution.
    J Theor Biol. 1990 Feb 22;142(4):485-501 PMID: 2338834
  24. CONFIDENCE LIMITS ON PHYLOGENIES: AN APPROACH USING THE BOOTSTRAP.
    Evolution. 1985 Jul;39(4):783-791 PMID: 28561359
  25. Campylobacter cinaedi (sp. nov.) and Campylobacter fennelliae (sp. nov.): two new Campylobacter species associated with enteric disease in homosexual men.
    J Infect Dis. 1985 Jan;151(1):131-9 PMID: 3965584
  26. Genes for gentamicin-(3)-N-acetyltransferases III and IV: I. Nucleotide sequence of the AAC(3)-IV gene and possible involvement of an IS140 element in its expression.
    Mol Gen Genet. 1984;193(1):179-87 PMID: 6318050
  27. Analysis of gene control signals by DNA fusion and cloning in Escherichia coli.
    J Mol Biol. 1980 Apr;138(2):179-207 PMID: 6997493
  28. Phylogeny of Helicobacter isolates from bird and swine feces and description of Helicobacter pametensis sp. nov.
    Int J Syst Bacteriol. 1994 Jul;44(3):553-60 PMID: 7520743
  29. Helicobacter bilis sp. nov., a novel Helicobacter species isolated from bile, livers, and intestines of aged, inbred mice.
    J Clin Microbiol. 1995 Feb;33(2):445-54 PMID: 7536217
  30. Helicobacter pylori requires an acidic environment to survive in the presence of urea.
    Infect Immun. 1995 May;63(5):1669-73 PMID: 7729871
  31. CLUSTAL V: multiple alignment of DNA and protein sequences.
    Methods Mol Biol. 1994;25:307-18 PMID: 8004173
  32. Helicobacter hepaticus sp. nov., a microaerophilic bacterium isolated from livers and intestinal mucosal scrapings from mice.
    J Clin Microbiol. 1994 May;32(5):1238-45 PMID: 8051250
  33. Effect of gastric pH on urease-dependent colonization of gnotobiotic piglets by Helicobacter pylori.
    Infect Immun. 1994 Sep;62(9):3604-7 PMID: 8063376
  34. Helicobacter canis sp. nov., a new species from dogs: an integrated study of phenotype and genotype.
    J Gen Microbiol. 1993 Oct;139(10):2495-504 PMID: 8254320
  35. Long term infection of the gastric mucosa with Helicobacter species does induce atrophic gastritis in an animal model of Helicobacter pylori infection.
    Zentralbl Bakteriol. 1993 Sep;280(1-2):38-50 PMID: 8280955
  36. Helicobacter acinonyx sp. nov., isolated from cheetahs with gastritis.
    Int J Syst Bacteriol. 1993 Jan;43(1):99-106 PMID: 8379970
  37. Cell kinetics of mucosal atrophy in rat stomach induced by long-term administration of ammonia.
    Gastroenterology. 1993 Mar;104(3):796-801 PMID: 8440436
  38. A standardized mouse model of Helicobacter pylori infection: introducing the Sydney strain.
    Gastroenterology. 1997 Apr;112(4):1386-97 PMID: 9098027
  39. The complete genome sequence of the gastric pathogen Helicobacter pylori.
    Nature. 1997 Aug 7;388(6642):539-47 PMID: 9252185
  40. BIONJ: an improved version of the NJ algorithm based on a simple model of sequence data.
    Mol Biol Evol. 1997 Jul;14(7):685-95 PMID: 9254330
  41. Helicobacter pylori.
    Clin Microbiol Rev. 1997 Oct;10(4):720-41 PMID: 9336670
  42. Identification and characterization of an aliphatic amidase in Helicobacter pylori.
    Mol Microbiol. 1997 Sep;25(5):989-98 PMID: 9364923
  43. Immune responses of specific-pathogen-free mice to chronic Helicobacter pylori (strain SS1) infection.
    Infect Immun. 1998 Apr;66(4):1349-55 PMID: 9529052
  44. Rectal and intranasal immunizations with recombinant urease induce distinct local and serum immune responses in mice and protect against Helicobacter pylori infection.
    Infect Immun. 1998 Jun;66(6):2879-86 PMID: 9596763
  45. The Helicobacter pylori UreI protein is not involved in urease activity but is essential for bacterial survival in vivo.
    Infect Immun. 1998 Sep;66(9):4517-21 PMID: 9712811
  46. In situ characterization of Helicobacter pylori arginase.
    Biochim Biophys Acta. 1998 Nov 10;1388(2):465-77 PMID: 9858781
  47. Genomic-sequence comparison of two unrelated isolates of the human gastric pathogen Helicobacter pylori.
    Nature. 1999 Jan 14;397(6715):176-80 PMID: 9923682
Article Info
Journal
Infection and immunity
Abbr.
Infect Immun
ISSN
0019-9567
Published
2003-10-00
Pages
5613-22
Language
English
Region
United States
NLM ID
0246127
PMCID
PMC201111
Subset
IM
Grants
NIAID NIH HHS · AI 38166 · United States
NIDDK NIH HHS · DK 53727 · United States
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