Programmed Death Ligand 1-Expressing Classical Dendritic Cells MitigateHelicobacter-Induced Gastritis

Cell Mol Gastroenterol Hepatol. 2021;12(2):715-739. doi: 10.1016/j.jcmgh.2021.04.007. Epub 2021 Apr 21.

Abstract

Background & aims: Helicobacter pylori has been reported to modulate local immune responses to colonize persistently in gastric mucosa. Although the induced expression of programmed cell death ligand 1 (PD-L1) has been suggested as an immune modulatory mechanism for persistent infection of H pylori, the main immune cells expressing PD-L1 and their functions in Helicobacter-induced gastritis still remain to be elucidated.

Methods: The blockades of PD-L1 with antibody or PD-L1-deficient bone marrow transplantation were performed in Helicobacter-infected mice. The main immune cells expressing PD-L1 in Helicobacter-infected stomach were determined by flow cytometry and immunofluorescence staining. Helicobacter felis or H pylori-infected dendritic cell (DC)-deficient mouse models including Flt3-/-, Zbtb46-diphtheria toxin receptor, and BDCA2-diphtheria toxin receptor mice were analyzed for pathologic changes and colonization levels. Finally, the location of PD-L1-expressing DCs and the correlation with H pylori infection were analyzed in human gastric tissues using multiplexed immunohistochemistry.

Results: Genetic or antibody-mediated blockade of PD-L1 aggravated Helicobacter-induced gastritis with mucosal metaplasia. Gastric classical DCs expressed considerably higher levels of PD-L1 than other immune cells and co-localized with T cells in gastritis lesions from Helicobacter-infected mice and human beings. H felis- or H pylori-infected Flt3-/- or classical DC-depleted mice showed aggravated gastritis with severe T-cell and neutrophil accumulation with low bacterial loads compared with that in control mice. Finally, PD-L1-expressing DCs were co-localized with T cells and showed a positive correlation with H pylori infection in human subjects.

Conclusions: The PD-1/PD-L1 pathway may be responsible for the immune modulatory function of gastric DCs that protects the gastric mucosa from Helicobacter-induced inflammation, but allows persistent Helicobacter colonization.

Keywords: Gastric Inflammation; Immune Regulation; Mucosal Metaplasia; T Cell.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Antibodies / pharmacology
  • B7-H1 Antigen / metabolism*
  • Bone Marrow Cells / drug effects
  • Bone Marrow Cells / metabolism
  • Bone Marrow Transplantation
  • CD11 Antigens / metabolism
  • CD8-Positive T-Lymphocytes / drug effects
  • CD8-Positive T-Lymphocytes / immunology
  • Dendritic Cells / metabolism*
  • Gastric Mucosa / drug effects
  • Gastric Mucosa / pathology
  • Gastritis / metabolism*
  • Gastritis / microbiology*
  • Gastritis / pathology
  • Helicobacter Infections / microbiology*
  • Helicobacter Infections / pathology
  • Helicobacter pylori / drug effects
  • Helicobacter pylori / physiology*
  • Inflammation / pathology
  • Male
  • Metaplasia
  • Mice
  • Mice, Inbred C57BL
  • T-Lymphocytes / immunology
  • fms-Like Tyrosine Kinase 3 / deficiency
  • fms-Like Tyrosine Kinase 3 / metabolism

Substances

  • Antibodies
  • B7-H1 Antigen
  • CD11 Antigens
  • Cd274 protein, mouse
  • Flt3 protein, mouse
  • fms-Like Tyrosine Kinase 3