Oral probiotic promotes indoleamine 2,3-dioxygenase- and TGF-β-Producing plasmacytoid dendritic cells to initiate protection against type 1 diabetes

Immunol Lett. 2021 Nov:239:12-19. doi: 10.1016/j.imlet.2021.07.009. Epub 2021 Jul 30.

Abstract

Colonization factor antigen I (CFA/I) fimbria, an adhesin from enterotoxigenic Escherichia coli, confers protection in murine autoimmune models for type 1 diabetes (T1D), multiple sclerosis, and rheumatoid arthritis. Although CFA/I fimbriae's initial mode of action is in a bystander or in an antigen (Ag)-independent fashion, protection is ultimately dependent upon the induction and/or activation of auto-Ag-specific regulatory T cells (Tregs). However, little is known about how protection transitions from bystander suppression to Ag-specific Tregs. Since dendritic cells (DCs) play an integral role in fate decisions for T cells becoming inflammatory or tolerogenic, the described study tests the hypothesis that Lactococcus lactis expressing CFA/I (LL-CFA/I) stimulates DCs to establish a regulatory microenvironment. To this end, bone marrow-derived dendritic cells (BMDCs) were infected in vitro with LL-CFA/I. Results revealed increased production of IL-10, TGF-β, and indoleamine 2,3-deoxygenase (IDO). Although co-culture of LL-CFA/I infected BMDCs with naïve T cells did not promote Foxp3 expression, TNF-α and IFN-γ production was suppressed. NOD mice orally dosed with LL-CFA/I showed an increase in regulatory plasmacytoid DCs (pDCs) expressing IDO and TGF-β in pancreatic lymph nodes (PaLNs) and spleen three days post-treatment. However, Tregs did not appear in the mucosal inductive sites until much later. These findings show that LL-CFA/I influences specific DC populations to establish tolerance.

Keywords: IDO; Plasmacytoid dendritic cells; Probiotic; Tolerance; Type 1 diabetes.

Publication types

  • Research Support, N.I.H., Extramural

MeSH terms

  • Administration, Oral
  • Animals
  • Antigens, Bacterial / genetics
  • Antigens, Bacterial / immunology
  • Antigens, Bacterial / metabolism
  • Blood Glucose / analysis
  • CD4-Positive T-Lymphocytes
  • Cells, Cultured
  • Coculture Techniques
  • Dendritic Cells / immunology*
  • Dendritic Cells / metabolism
  • Diabetes Mellitus, Type 1 / diagnosis
  • Diabetes Mellitus, Type 1 / genetics
  • Diabetes Mellitus, Type 1 / immunology
  • Diabetes Mellitus, Type 1 / prevention & control*
  • Disease Models, Animal
  • Female
  • Fimbriae Proteins / genetics
  • Fimbriae Proteins / immunology
  • Fimbriae Proteins / metabolism
  • Humans
  • Indoleamine-Pyrrole 2,3,-Dioxygenase / metabolism
  • Lactococcus lactis / genetics
  • Lactococcus lactis / immunology*
  • Lactococcus lactis / metabolism
  • Lymph Nodes / cytology
  • Mice
  • Mice, Transgenic
  • Primary Cell Culture
  • Probiotics / administration & dosage*
  • Spleen / cytology
  • Transforming Growth Factor beta / metabolism

Substances

  • Antigens, Bacterial
  • Blood Glucose
  • Indoleamine-Pyrrole 2,3,-Dioxygenase
  • Transforming Growth Factor beta
  • colonization factor antigens
  • Fimbriae Proteins