Home LiteratureArticle Details
PMID: 11238562 Published · ppublish English Journal Article Research Support, U.S. Gov't, Non-P.H.S. Research Support, U.S. Gov't, P.H.S.

Helicobacter pylori strain-specific differences in genetic content, identified by microarray, influence host inflammatory responses.

The Journal of clinical investigation ·Vol. 107 ·No. 5 ·2001-03-00 ·Pages 611-20

Israel DA, Salama N, Arnold CN, Moss SF, Ando T, Wirth HP, Tham KT, Camorlinga M, Blaser MJ, Falkow S, Peek RM

Abstract

Helicobacter pylori enhances the risk for ulcer disease and gastric cancer, yet only a minority of H. pylori-colonized individuals develop disease. We examined the ability of two H. pylori isolates to induce differential host responses in vivo or in vitro, and then used an H. pylori whole genome microarray to identify bacterial determinants related to pathogenesis. Gastric ulcer strain B128 induced more severe gastritis, proliferation, and apoptosis in gerbil mucosa than did duodenal ulcer strain G1.1, and gastric ulceration and atrophy occurred only in B128+ gerbils. In vitro, gerbil-passaged B128 derivatives significantly increased IL-8 secretion and apoptosis compared with G1.1 strains. DNA hybridization to the microarray identified several strain-specific differences in gene composition including a large deletion of the cag pathogenicity island in strain G1.1. Partial and complete disruption of the cag island in strain B128 attenuated induction of IL-8 in vitro and significantly decreased gastric inflammation in vivo. These results indicate that the ability of H. pylori to regulate epithelial cell responses related to inflammation depends on the presence of an intact cag pathogenicity island. Use of an H pylori whole genome microarray is an effective method to identify differences in gene content between H. pylori strains that induce distinct pathological outcomes in a rodent model of H. pylori infection.

MeSH Terms
Animals Antigens, Bacterial Apoptosis Bacterial Proteins/genetics Cell Division Cell Line Duodenal Ulcer/metabolism,pathology Gastric Mucosa/metabolism,pathology Gastritis/etiology,metabolism Genome, Bacterial Gerbillinae Helicobacter Infections/metabolism,pathology Helicobacter pylori/genetics,pathogenicity Humans Inflammation/pathology Interleukin-8/biosynthesis Oligonucleotide Array Sequence Analysis Sequence Deletion Stomach Ulcer/metabolism,pathology
Chemicals
Antigens, Bacterial Bacterial Proteins Interleukin-8 cagA protein, Helicobacter pylori
Authors & Affiliations
11 authors, click to expand affiliations / ORCID
Israel D A
Division of Gastroenterology, Vanderbilt University School of Medicine, Nashville, Tennessee, USA.
Salama N
Arnold C N
Moss S F
Ando T
Wirth H P
Tham K T
Camorlinga M
Blaser M J
Falkow S
Peek R M
References (52)
52 references, click to expand
  1. Altered states: involvement of phosphorylated CagA in the induction of host cellular growth changes by Helicobacter pylori.
    Proc Natl Acad Sci U S A. 1999 Dec 7;96(25):14559-64 PMID: 10588744
  2. Heightened inflammatory response and cytokine expression in vivo to cagA+ Helicobacter pylori strains.
    Lab Invest. 1995 Dec;73(6):760-70 PMID: 8558837
  3. Helicobacter pylori strain-specific genotypes and modulation of the gastric epithelial cell cycle.
    Cancer Res. 1999 Dec 15;59(24):6124-31 PMID: 10626802
  4. Sequence analysis and clinical significance of the iceA gene from Helicobacter pylori strains in Japan.
    J Clin Microbiol. 2000 Feb;38(2):483-8 PMID: 10655332
  5. Tyrosine phosphorylation of the Helicobacter pylori CagA antigen after cag-driven host cell translocation.
    Proc Natl Acad Sci U S A. 2000 Feb 1;97(3):1263-8 PMID: 10655519
  6. Helicobacter-specific cell-mediated immune responses display a predominant Th1 phenotype and promote a delayed-type hypersensitivity response in the stomachs of mice.
    J Immunol. 1996 Jun 15;156(12):4729-38 PMID: 8648119
  7. The risk of stomach cancer in patients with gastric or duodenal ulcer disease.
    N Engl J Med. 1996 Jul 25;335(4):242-9 PMID: 8657240
  8. Induction of gastric epithelial apoptosis by Helicobacter pylori.
    Gut. 1996 Apr;38(4):498-501 PMID: 8707076
  9. Helicobacter pylori picB, a homologue of the Bordetella pertussis toxin secretion protein, is required for induction of IL-8 in gastric epithelial cells.
    Mol Microbiol. 1995 Dec;18(5):867-76 PMID: 8825091
  10. cag, a pathogenicity island of Helicobacter pylori, encodes type I-specific and disease-associated virulence factors.
    Proc Natl Acad Sci U S A. 1996 Dec 10;93(25):14648-53 PMID: 8962108
  11. Helicobacter pylori cagA+ strains and dissociation of gastric epithelial cell proliferation from apoptosis.
    J Natl Cancer Inst. 1997 Jun 18;89(12):863-8 PMID: 9196252
  12. The complete genome sequence of the gastric pathogen Helicobacter pylori.
    Nature. 1997 Aug 7;388(6642):539-47 PMID: 9252185
  13. Helicobacter pylori infection activates NF-kappa B in gastric epithelial cells.
    Gastroenterology. 1997 Oct;113(4):1099-109 PMID: 9322504
  14. High seropositivity of anti-CagA antibody in Helicobacter pylori-infected patients irrelevant to peptic ulcers and normal mucosa in Japan.
    Dig Dis Sci. 1997 Sep;42(9):1841-7 PMID: 9331145
  15. Regulation of gastric epithelial cell growth by Helicobacter pylori: offdence for a major role of apoptosis.
    Gastroenterology. 1997 Dec;113(6):1836-47 PMID: 9394723
  16. Murine CD4 T-cell response to Helicobacter infection: TH1 cells enhance gastritis and TH2 cells reduce bacterial load.
    Gastroenterology. 1997 Dec;113(6):1848-57 PMID: 9394724
  17. Lymphocytes in the human gastric mucosa during Helicobacter pylori have a T helper cell 1 phenotype.
    Gastroenterology. 1998 Mar;114(3):482-92 PMID: 9496938
  18. Mice lacking secretory phospholipase A2 show altered apoptosis and differentiation with Helicobacter felis infection.
    Gastroenterology. 1998 Apr;114(4):675-89 PMID: 9516388
  19. Epithelial attachment alters the outcome of Helicobacter pylori infection.
    Proc Natl Acad Sci U S A. 1998 Mar 31;95(7):3925-30 PMID: 9520469
  20. Analyses of the cag pathogenicity island of Helicobacter pylori.
    Mol Microbiol. 1998 Apr;28(1):37-53 PMID: 9593295
  21. Clinical relevance of the cagA, vacA, and iceA status of Helicobacter pylori.
    Gastroenterology. 1998 Jul;115(1):58-66 PMID: 9649459
  22. Helicobacter pylori infection induces gastric cancer in mongolian gerbils.
    Gastroenterology. 1998 Sep;115(3):642-8 PMID: 9721161
  23. Experimental infection of Mongolian gerbils with wild-type and mutant Helicobacter pylori strains.
    Infect Immun. 1998 Oct;66(10):4856-66 PMID: 9746590
  24. PCR-based subtractive hybridization and differences in gene content among strains of Helicobacter pylori.
    Proc Natl Acad Sci U S A. 1998 Oct 27;95(22):13108-13 PMID: 9789049
  25. Adherence to gastric epithelial cells induces expression of a Helicobacter pylori gene, iceA, that is associated with clinical outcome.
    Proc Assoc Am Physicians. 1998 Nov-Dec;110(6):531-44 PMID: 9824536
  26. Cluster analysis and display of genome-wide expression patterns.
    Proc Natl Acad Sci U S A. 1998 Dec 8;95(25):14863-8 PMID: 9843981
  27. Role of gamma interferon in Helicobacter pylori-induced gastric inflammatory responses in a mouse model.
    Infect Immun. 1999 Jan;67(1):279-85 PMID: 9864227
  28. Genomic-sequence comparison of two unrelated isolates of the human gastric pathogen Helicobacter pylori.
    Nature. 1999 Jan 14;397(6715):176-80 PMID: 9923682
  29. Healing of Helicobacter pylori-induced gastric ulcers in Mongolian gerbils: combined treatment with omeprazole and clarithromycin.
    Dig Dis Sci. 1999 Feb;44(2):257-65 PMID: 10063909
  30. DNA arrays for analysis of gene expression.
    Methods Enzymol. 1999;303:179-205 PMID: 10349646
  31. Helicobacter pylori CagA protein can be tyrosine phosphorylated in gastric epithelial cells.
    J Exp Med. 2000 Feb 21;191(4):593-602 PMID: 10684851
  32. Translocation of Helicobacter pylori CagA into gastric epithelial cells by type IV secretion.
    Science. 2000 Feb 25;287(5457):1497-500 PMID: 10688800
  33. Interleukin-1 polymorphisms associated with increased risk of gastric cancer.
    Nature. 2000 Mar 23;404(6776):398-402 PMID: 10746728
  34. Concurrent enteric helminth infection modulates inflammation and gastric immune responses and reduces helicobacter-induced gastric atrophy.
    Nat Med. 2000 May;6(5):536-42 PMID: 10802709
  35. Helicobacter pylori modulates lymphoepithelial cell interactions leading to epithelial cell damage through Fas/Fas ligand interactions.
    Infect Immun. 2000 Jul;68(7):4303-11 PMID: 10858249
  36. Helicobacter pylori-induced mucosal inflammation is Th1 mediated and exacerbated in IL-4, but not IFN-gamma, gene-deficient mice.
    J Immunol. 2000 Jul 15;165(2):1022-9 PMID: 10878379
  37. Helicobacter pylori urease binds to class II MHC on gastric epithelial cells and induces their apoptosis.
    J Immunol. 2000 Aug 15;165(4):1918-24 PMID: 10925273
  38. Identification of type II restriction and modification systems in Helicobacter pylori reveals their substantial diversity among strains.
    Proc Natl Acad Sci U S A. 2000 Aug 15;97(17):9671-6 PMID: 10944229
  39. In vivo disruption of the fas pathway abrogates gastric growth alterations secondary to Helicobacter infection.
    J Infect Dis. 2000 Sep;182(3):856-64 PMID: 10950781
  40. Restriction-modification system differences in Helicobacter pylori are a barrier to interstrain plasmid transfer.
    Mol Microbiol. 2000 Sep;37(5):1052-65 PMID: 10972824
  41. A whole-genome microarray reveals genetic diversity among Helicobacter pylori strains.
    Proc Natl Acad Sci U S A. 2000 Dec 19;97(26):14668-73 PMID: 11121067
  42. Gastric precancerous process in a high risk population: cohort follow-up.
    Cancer Res. 1990 Aug 1;50(15):4737-40 PMID: 2369748
  43. Helicobacter pylori and peptic ulcer disease.
    N Engl J Med. 1991 Apr 11;324(15):1043-8 PMID: 2005942
  44. Mucosal IgA recognition of Helicobacter pylori 120 kDa protein, peptic ulceration, and gastric pathology.
    Lancet. 1991 Aug 10;338(8763):332-5 PMID: 1677696
  45. Helicobacter pylori infection and the risk of gastric carcinoma.
    N Engl J Med. 1991 Oct 17;325(16):1127-31 PMID: 1891020
  46. Helicobacter pylori infection and gastric carcinoma among Japanese Americans in Hawaii.
    N Engl J Med. 1991 Oct 17;325(16):1132-6 PMID: 1891021
  47. Gastric interleukin-8 and IgA IL-8 autoantibodies in Helicobacter pylori infection.
    Scand J Immunol. 1993 Jan;37(1):65-70 PMID: 8418474
  48. Systemic and mucosal humoral responses to Helicobacter pylori in gastric cancer.
    Gut. 1993 Oct;34(10):1339-43 PMID: 8244098
  49. Infection with Helicobacter pylori strains possessing cagA is associated with an increased risk of developing adenocarcinoma of the stomach.
    Cancer Res. 1995 May 15;55(10):2111-5 PMID: 7743510
  50. Mosaicism in vacuolating cytotoxin alleles of Helicobacter pylori. Association of specific vacA types with cytotoxin production and peptic ulceration.
    J Biol Chem. 1995 Jul 28;270(30):17771-7 PMID: 7629077
  51. Helicobacter pylori and atrophic gastritis: importance of the cagA status.
    J Natl Cancer Inst. 1995 Dec 6;87(23):1777-80 PMID: 7473834
  52. Helicobacter pylori alters gastric epithelial cell cycle events and gastrin secretion in Mongolian gerbils.
    Gastroenterology. 2000 Jan;118(1):48-59 PMID: 10611153
Article Info
Journal
The Journal of clinical investigation
Abbr.
J Clin Invest
ISSN
0021-9738
Published
2001-03-00
Pages
611-20
Language
English
Region
United States
NLM ID
7802877
PMCID
PMC199426
Subset
IM
Grants
NIAID NIH HHS · R01 AI38459 · United States
NCI NIH HHS · R29 CA077955 · United States
NIDDK NIH HHS · KO8 DK02381 · United States
NCI NIH HHS · R29 CA77955 · United States
NIAID NIH HHS · R01 AI038459 · United States
NIDDK NIH HHS · R01 DK50837 · United States
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: [email protected]