Antigen-specific Helios- , Neuropilin-1- Tregs induce apoptosis of autoreactive B cells via PD-L1

Immunol Cell Biol. 2018 Sep;96(8):852-862. doi: 10.1111/imcb.12053. Epub 2018 May 2.

Abstract

Regulatory T cells (Tregs) maintain self-tolerance and prevent autoimmunity by controlling autoreactive T cells. We recently demonstrated in vivo that Tregs can directly suppress auto-reactive B cells via programmed death ligand 1 (PD-L1) that ligated PD-1 on B cells and caused them to undergo apoptosis. Here, we asked whether this mechanism is utilized by thymus-derived natural Tregs and/or by peripheral lymphoid tissue-induced Tregs. We first demonstrated that antigen-specific PD-L1-expressing Tregs were induced in the draining lymph node of autoantigen-expressing tissue and characterized them by their lack of the transcription factor Helios and of the surface marker Neuropilin-1 (Nrp-1). Next, we established an in vitro co-culture system to study the interaction between B cells and Treg subsets under controlled conditions. We found that Nrp- Treg, but not Nrp+ Treg suppressed autoreactive B cells, whereas both were able to suppress T-helper cells. Such suppression was antigen-specific and was facilitated by PD-L1/PD-1-induced apoptosis. Furthermore, it required physical cell contact and was MHC II-restricted, providing an explanation for the antigen-specificity of peripherally-induced Tregs. These findings identify a role for peripherally induced Helios- Nrp-1- inducible Treg in controlling peripheral B-cell tolerance against tissue auto-antigens.

Keywords: Apoptosis; B cells; Helios; Neuropilin-1; PD-1; Treg.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Apoptosis
  • Autoantigens / immunology
  • Autoimmunity
  • B-Lymphocytes / immunology*
  • B7-H1 Antigen / metabolism*
  • DNA-Binding Proteins / metabolism
  • Forkhead Transcription Factors / metabolism
  • Humans
  • Mice
  • Mice, Inbred C57BL
  • Mice, Transgenic
  • Neuropilin-1 / metabolism
  • Self Tolerance
  • T-Lymphocytes, Regulatory / immunology*
  • Transcription Factors / metabolism

Substances

  • Autoantigens
  • B7-H1 Antigen
  • DNA-Binding Proteins
  • Forkhead Transcription Factors
  • Foxp3 protein, mouse
  • Transcription Factors
  • Zfpn1a2 protein, mouse
  • Neuropilin-1