IL-22-induced antimicrobial peptides are key determinants of mucosal vaccine-induced protection against H. pylori in mice

Mucosal Immunol. 2017 Jan;10(1):271-281. doi: 10.1038/mi.2016.38. Epub 2016 May 4.

Abstract

Despite the recent description of the mucosal vaccine-induced reduction of Helicobacter pylori natural infection in a phase 3 clinical trial, the absence of immune correlates of protection slows the final development of the vaccine. In this study, we evaluated the role of interleukin (IL)-22 in mucosal vaccine-induced protection. Gastric IL-22 levels were increased in mice intranasally immunized with urease+cholera toxin and challenged with H. felis, as compared with controls. Flow cytometry analysis showed that a peak of CD4+IL-22+IL-17+ T cells infiltrating the gastric mucosa occurred in immunized mice in contrast to control mice. The inhibition of the IL-22 biological activity prevented the vaccine-induced reduction of H. pylori infection. Remarkably, anti-microbial peptides (AMPs) extracted from the stomachs of vaccinated mice, but not from the stomachs of non-immunized or immunized mice, injected with anti-IL-22 antibodies efficiently killed H. pylori in vitro. Finally, H. pylori infection in vaccinated RegIIIβ-deficient mice was not reduced as efficiently as in wild-type mice. These results demonstrate that IL-22 has a critical role in vaccine-induced protection, by promoting the expression of AMPs, such as RegIIIβ, capable of killing Helicobacter. Therefore, it can be concluded that urease-specific memory Th17/Th22 cells could constitute immune correlates of vaccine protection in humans.

MeSH terms

  • Animals
  • Antigens, Bacterial / immunology*
  • Antimicrobial Cationic Peptides / genetics
  • Antimicrobial Cationic Peptides / metabolism
  • Bacterial Vaccines / immunology*
  • Cells, Cultured
  • Disease Models, Animal
  • Female
  • Gene Expression Regulation
  • Helicobacter Infections / immunology*
  • Helicobacter Infections / prevention & control
  • Helicobacter pylori / immunology*
  • Humans
  • Interleukin-22
  • Interleukins / genetics
  • Interleukins / metabolism*
  • Mice
  • Mice, Inbred BALB C
  • Mice, Inbred C57BL
  • Mice, Knockout
  • Mucous Membrane / immunology*
  • Mucous Membrane / microbiology
  • Pancreatitis-Associated Proteins
  • Proteins / genetics
  • Proteins / metabolism
  • Th17 Cells / immunology*
  • Urease / immunology*

Substances

  • Antigens, Bacterial
  • Antimicrobial Cationic Peptides
  • Bacterial Vaccines
  • Interleukins
  • Pancreatitis-Associated Proteins
  • Proteins
  • Reg3b protein, mouse
  • Urease