Skip to main content
Infection and Immunity logoLink to Infection and Immunity
. 1993 Jun;61(6):2309–2315. doi: 10.1128/iai.61.6.2309-2315.1993

Local and systemic immune responses in murine Helicobacter felis active chronic gastritis.

J G Fox 1, M Blanco 1, J C Murphy 1, N S Taylor 1, A Lee 1, Z Kabok 1, J Pappo 1
PMCID: PMC280850  PMID: 8500873

Abstract

Helicobacter felis inoculated per os into germfree mice and their conventional non-germfree counterparts caused a persistent chronic gastritis of approximately 1 year in duration. Mononuclear leukocytes were the predominant inflammatory cell throughout the study, although polymorphonuclear cell infiltrates were detected as well. Immunohistochemical analyses of gastric mucosa from H. felis-infected mice revealed the presence of mucosal B220+ cells coalescing into lymphoid follicles surrounded by aggregates of Thy-1.2+ T cells; CD4+, CD5+, and alpha beta T cells predominated in organized gastric mucosal and submucosal lymphoid tissue, and CD11b+ cells occurred frequently in the mucosa. Follicular B cells comprised immunoglobulin M+ (IgM+) and IgA+ cells. Numerous IgA-producing B cells were present in the gastric glands, the lamina propria, and gastric epithelium. Infected animals developed anti-H. felis serum IgM antibody responses up to 8 weeks postinfection and significant levels of IgG anti-H. felis antibody in serum, which remained elevated throughout the 50-week course of the study.

Full text

PDF
2309

Images in this article

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Baskerville A., Newell D. G. Naturally occurring chronic gastritis and C pylori infection in the rhesus monkey: a potential model for gastritis in man. Gut. 1988 Apr;29(4):465–472. doi: 10.1136/gut.29.4.465. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Blaser M. J. Hypotheses on the pathogenesis and natural history of Helicobacter pylori-induced inflammation. Gastroenterology. 1992 Feb;102(2):720–727. doi: 10.1016/0016-5085(92)90126-j. [DOI] [PubMed] [Google Scholar]
  3. Chen M., Lee A., Hazell S. Immunisation against gastric helicobacter infection in a mouse/Helicobacter felis model. Lancet. 1992 May 2;339(8801):1120–1121. doi: 10.1016/0140-6736(92)90720-n. [DOI] [PubMed] [Google Scholar]
  4. Correa P., Fox J., Fontham E., Ruiz B., Lin Y. P., Zavala D., Taylor N., Mackinley D., de Lima E., Portilla H. Helicobacter pylori and gastric carcinoma. Serum antibody prevalence in populations with contrasting cancer risks. Cancer. 1990 Dec 15;66(12):2569–2574. doi: 10.1002/1097-0142(19901215)66:12<2569::aid-cncr2820661220>3.0.co;2-i. [DOI] [PubMed] [Google Scholar]
  5. Crabtree J. E., Shallcross T. M., Heatley R. V., Wyatt J. I. Mucosal tumour necrosis factor alpha and interleukin-6 in patients with Helicobacter pylori associated gastritis. Gut. 1991 Dec;32(12):1473–1477. doi: 10.1136/gut.32.12.1473. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Crabtree J. E., Shallcross T. M., Wyatt J. I., Taylor J. D., Heatley R. V., Rathbone B. J., Losowsky M. S. Mucosal humoral immune response to Helicobacter pylori in patients with duodenitis. Dig Dis Sci. 1991 Sep;36(9):1266–1273. doi: 10.1007/BF01307520. [DOI] [PubMed] [Google Scholar]
  7. Czinn S. J., Dahms B. B., Jacobs G. H., Kaplan B., Rothstein F. C. Campylobacter-like organisms in association with symptomatic gastritis in children. J Pediatr. 1986 Jul;109(1):80–83. doi: 10.1016/s0022-3476(86)80579-0. [DOI] [PubMed] [Google Scholar]
  8. Czinn S. J., Nedrud J. G. Oral immunization against Helicobacter pylori. Infect Immun. 1991 Jul;59(7):2359–2363. doi: 10.1128/iai.59.7.2359-2363.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Engstrand L., Scheynius A., Påhlson C. An increased number of gamma/delta T-cells and gastric epithelial cell expression of the groEL stress-protein homologue in Helicobacter pylori-associated chronic gastritis of the antrum. Am J Gastroenterol. 1991 Aug;86(8):976–980. [PubMed] [Google Scholar]
  10. Ermak T. H., Owen R. L. Differential distribution of lymphocytes and accessory cells in mouse Peyer's patches. Anat Rec. 1986 Jun;215(2):144–152. doi: 10.1002/ar.1092150208. [DOI] [PubMed] [Google Scholar]
  11. Fox J. G., Correa P., Taylor N. S., Lee A., Otto G., Murphy J. C., Rose R. Helicobacter mustelae-associated gastritis in ferrets. An animal model of Helicobacter pylori gastritis in humans. Gastroenterology. 1990 Aug;99(2):352–361. doi: 10.1016/0016-5085(90)91016-y. [DOI] [PubMed] [Google Scholar]
  12. Fox J. G., Lee A., Otto G., Taylor N. S., Murphy J. C. Helicobacter felis gastritis in gnotobiotic rats: an animal model of Helicobacter pylori gastritis. Infect Immun. 1991 Mar;59(3):785–791. doi: 10.1128/iai.59.3.785-791.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Fox J. G., Otto G., Murphy J. C., Taylor N. S., Lee A. Gastric colonization of the ferret with Helicobacter species: natural and experimental infections. Rev Infect Dis. 1991 Jul-Aug;13 (Suppl 8):S671–S680. doi: 10.1093/clinids/13.supplement_8.s671. [DOI] [PubMed] [Google Scholar]
  14. Fox J. G., Paster B. J., Dewhirst F. E., Taylor N. S., Yan L. L., Macuch P. J., Chmura L. M. Helicobacter mustelae isolation from feces of ferrets: evidence to support fecal-oral transmission of a gastric Helicobacter. Infect Immun. 1992 Feb;60(2):606–611. doi: 10.1128/iai.60.2.606-611.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Fujihashi K., Taguchi T., Aicher W. K., McGhee J. R., Bluestone J. A., Eldridge J. H., Kiyono H. Immunoregulatory functions for murine intraepithelial lymphocytes: gamma/delta T cell receptor-positive (TCR+) T cells abrogate oral tolerance, while alpha/beta TCR+ T cells provide B cell help. J Exp Med. 1992 Mar 1;175(3):695–707. doi: 10.1084/jem.175.3.695. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Goodman T., Lefrançois L. Expression of the gamma-delta T-cell receptor on intestinal CD8+ intraepithelial lymphocytes. Nature. 1988 Jun 30;333(6176):855–858. doi: 10.1038/333855a0. [DOI] [PubMed] [Google Scholar]
  17. Graham D. Y., Lew G. M., Klein P. D., Evans D. G., Evans D. J., Jr, Saeed Z. A., Malaty H. M. Effect of treatment of Helicobacter pylori infection on the long-term recurrence of gastric or duodenal ulcer. A randomized, controlled study. Ann Intern Med. 1992 May 1;116(9):705–708. doi: 10.7326/0003-4819-116-9-705. [DOI] [PubMed] [Google Scholar]
  18. Hazell S. L., Borody T. J., Gal A., Lee A. Campylobacter pyloridis gastritis I: Detection of urease as a marker of bacterial colonization and gastritis. Am J Gastroenterol. 1987 Apr;82(4):292–296. [PubMed] [Google Scholar]
  19. Krakowka S., Morgan D. R., Kraft W. G., Leunk R. D. Establishment of gastric Campylobacter pylori infection in the neonatal gnotobiotic piglet. Infect Immun. 1987 Nov;55(11):2789–2796. doi: 10.1128/iai.55.11.2789-2796.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. LOWRY O. H., ROSEBROUGH N. J., FARR A. L., RANDALL R. J. Protein measurement with the Folin phenol reagent. J Biol Chem. 1951 Nov;193(1):265–275. [PubMed] [Google Scholar]
  21. Lee A., Fox J. G., Otto G., Murphy J. A small animal model of human Helicobacter pylori active chronic gastritis. Gastroenterology. 1990 Nov;99(5):1315–1323. doi: 10.1016/0016-5085(90)91156-z. [DOI] [PubMed] [Google Scholar]
  22. Lee A., Hazell S. L., O'Rourke J., Kouprach S. Isolation of a spiral-shaped bacterium from the cat stomach. Infect Immun. 1988 Nov;56(11):2843–2850. doi: 10.1128/iai.56.11.2843-2850.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Lee A., Krakowka S., Fox J. G., Otto G., Eaton K. A., Murphy J. C. Role of Helicobacter felis in chronic canine gastritis. Vet Pathol. 1992 Nov;29(6):487–494. doi: 10.1177/030098589202900601. [DOI] [PubMed] [Google Scholar]
  24. Mai U. E., Perez-Perez G. I., Allen J. B., Wahl S. M., Blaser M. J., Smith P. D. Surface proteins from Helicobacter pylori exhibit chemotactic activity for human leukocytes and are present in gastric mucosa. J Exp Med. 1992 Feb 1;175(2):517–525. doi: 10.1084/jem.175.2.517. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Marshall B. J., Warren J. R. Unidentified curved bacilli in the stomach of patients with gastritis and peptic ulceration. Lancet. 1984 Jun 16;1(8390):1311–1315. doi: 10.1016/s0140-6736(84)91816-6. [DOI] [PubMed] [Google Scholar]
  26. Nielsen H., Andersen L. P. Chemotactic activity of Helicobacter pylori sonicate for human polymorphonuclear leucocytes and monocytes. Gut. 1992 Jun;33(6):738–742. doi: 10.1136/gut.33.6.738. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Nomura A., Stemmermann G. N., Chyou P. H., Kato I., Perez-Perez G. I., Blaser M. J. Helicobacter pylori infection and gastric carcinoma among Japanese Americans in Hawaii. N Engl J Med. 1991 Oct 17;325(16):1132–1136. doi: 10.1056/NEJM199110173251604. [DOI] [PubMed] [Google Scholar]
  28. Pappo J. Generation and characterization of monoclonal antibodies recognizing follicle epithelial M cells in rabbit gut-associated lymphoid tissues. Cell Immunol. 1989 Apr 15;120(1):31–41. doi: 10.1016/0008-8749(89)90172-x. [DOI] [PubMed] [Google Scholar]
  29. Parsonnet J., Friedman G. D., Vandersteen D. P., Chang Y., Vogelman J. H., Orentreich N., Sibley R. K. Helicobacter pylori infection and the risk of gastric carcinoma. N Engl J Med. 1991 Oct 17;325(16):1127–1131. doi: 10.1056/NEJM199110173251603. [DOI] [PubMed] [Google Scholar]
  30. Paster B. J., Lee A., Fox J. G., Dewhirst F. E., Tordoff L. A., Fraser G. J., O'Rourke J. L., Taylor N. S., Ferrero R. Phylogeny of Helicobacter felis sp. nov., Helicobacter mustelae, and related bacteria. Int J Syst Bacteriol. 1991 Jan;41(1):31–38. doi: 10.1099/00207713-41-1-31. [DOI] [PubMed] [Google Scholar]
  31. Radin M. J., Eaton K. A., Krakowka S., Morgan D. R., Lee A., Otto G., Fox J. Helicobacter pylori gastric infection in gnotobiotic beagle dogs. Infect Immun. 1990 Aug;58(8):2606–2612. doi: 10.1128/iai.58.8.2606-2612.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Stohrer R., Kearney J. F. Fine idiotype analysis of B cell precursors in the T-dependent and T-independent responses to alpha 1-3 dextran in BALB/c mice. J Exp Med. 1983 Dec 1;158(6):2081–2094. doi: 10.1084/jem.158.6.2081. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Trejdosiewicz L. K., Calabrese A., Smart C. J., Oakes D. J., Howdle P. D., Crabtree J. E., Losowsky M. S., Lancaster F., Boylston A. W. Gamma delta T cell receptor-positive cells of the human gastrointestinal mucosa: occurrence and V region gene expression in Heliobacter pylori-associated gastritis, coeliac disease and inflammatory bowel disease. Clin Exp Immunol. 1991 Jun;84(3):440–444. [PMC free article] [PubMed] [Google Scholar]
  34. Weisz-Carrington P., Roux M. E., McWilliams M., PHILLIPS-Quagliata J. M., Lamm M. E. Organ and isotype distribution of plasma cells producing specific antibody after oral immunization: evidence for a generalized secretory immune system. J Immunol. 1979 Oct;123(4):1705–1708. [PubMed] [Google Scholar]

Articles from Infection and Immunity are provided here courtesy of American Society for Microbiology (ASM)

RESOURCES