Protection against Helicobacter pylori infection following immunization is IL-12-dependent and mediated by Th1 cells

J Immunol. 2002 Dec 15;169(12):6977-84. doi: 10.4049/jimmunol.169.12.6977.

Abstract

The regulatory roles of Th1 and Th2 cells in immune protection against Helicobacter infection are not clearly understood. In this study, we report that a primary H. pylori infection can be established in the absence of IL-12 or IFN-gamma. However, IFN-gamma, but not IL-12, was involved in the development of gastritis because IFN-gamma(-/-) (GKO) mice exhibited significantly less inflammation as compared with IL-12(-/-) or wild-type (WT) mice. Both IL-12(-/-) and GKO mice failed to develop protection following oral immunization with H. pylori lysate and cholera toxin adjuvant. By contrast, Th2-deficient, IL-4(-/-), and WT mice were equally well protected. Mucosal immunization in the presence of coadministered rIL-12 in WT mice increased Ag-specific IFN-gamma-producing T cells by 5-fold and gave an additional 4-fold reduction in colonizing bacteria, confirming a key role of Th1 cells in protection. Importantly, only protected IL-4(-/-) and WT mice demonstrated substantial influx of CD4(+) T cells in the gastric mucosa. The extent of inflammation in challenged IL-12(-/-) and GKO mice was much reduced compared with that in WT mice, indicating that IFN-gamma/Th1 cells also play a major role in postimmunization gastritis. Of note, postimmunization gastritis in IL-4(-/-) mice was significantly milder than WT mice, despite a similar level of protection, indicating that immune protection is not directly linked to the degree of gastric inflammation. Only protected mice had T cells that produced high levels of IFN-gamma to recall Ag, whereas both protected and unprotected mice produced high levels of IL-13. We conclude that IL-12 and Th1 responses are crucial for H. pylori-specific protective immunity.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Antibodies, Bacterial / biosynthesis
  • Antibodies, Bacterial / blood
  • Epitopes, T-Lymphocyte / immunology
  • Gastritis / genetics
  • Gastritis / immunology
  • Helicobacter Infections / genetics
  • Helicobacter Infections / immunology*
  • Helicobacter Infections / prevention & control*
  • Helicobacter pylori / immunology*
  • Immunization, Secondary
  • Immunoglobulin A / biosynthesis
  • Immunoglobulin A / blood
  • Immunoglobulin G / biosynthesis
  • Immunoglobulin G / blood
  • Interferon-gamma / biosynthesis
  • Interferon-gamma / deficiency
  • Interferon-gamma / genetics
  • Interleukin-12 / deficiency
  • Interleukin-12 / genetics
  • Interleukin-12 / physiology*
  • Lymphopenia / genetics
  • Lymphopenia / immunology
  • Mice
  • Mice, Inbred C57BL
  • Mice, Knockout
  • Th1 Cells / immunology*
  • Th1 Cells / metabolism
  • Th1 Cells / pathology
  • Th2 Cells / immunology
  • Vaccination*

Substances

  • Antibodies, Bacterial
  • Epitopes, T-Lymphocyte
  • Immunoglobulin A
  • Immunoglobulin G
  • Interleukin-12
  • Interferon-gamma