Posttranslational modification of HLA-DQ binding islet autoantigens in type 1 diabetes

Diabetes. 2014 Jan;63(1):237-47. doi: 10.2337/db12-1214. Epub 2013 Oct 2.

Abstract

Posttranslational modification (PTM) of islet autoantigens can cause lack of central tolerance in type 1 diabetes (T1D). Tissue transglutaminase (tTG), involved in PTM of gluten antigens in celiac disease, creates negatively charged peptides favored by T1D-predisposing HLA-DQ molecules, offering an attractive candidate modifying islet autoantigens in T1D. The highly predisposing HLA-DQ8cis/trans molecules share preferences for negatively charged peptides, as well as distinct peptide-binding characteristics that distinguish their peptide-binding repertoire. We screened islet autoantigens with the tTG substrate motif for candidate-modified epitopes binding to HLA-DQ8cis/trans and identified 31 candidate islet epitopes. Deamidation was confirmed for 28 peptides (90%). Two of these epitopes preferentially bound to HLA-DQ8cis and six to HLA-DQ8trans upon deamidation, whereas all other peptides bound equally to HLA-DQ8cis/trans. HLA-DQ8cis-restricted T cells from a new-onset T1D patient could only be generated against a deamidated proinsulin peptide, but cross-reacted with native proinsulin peptide upon restimulation. The rate of T-cell autoreactivity in recent-onset T1D patients extended from 42% to native insulin to 68% adding responses to modified proinsulin, versus 20% and 37% respectively, in healthy donors. Most patients responded by interferon-γ, whereas most healthy donors produced interleukin-10 only. Thus, T-cell autoreactivity exists to modified islet epitopes that differs in quality and quantity between patients and healthy donors.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Autoantigens / genetics
  • Autoantigens / immunology
  • Autoantigens / metabolism*
  • Child
  • Diabetes Mellitus, Type 1 / genetics
  • Diabetes Mellitus, Type 1 / immunology
  • Diabetes Mellitus, Type 1 / metabolism*
  • Epitopes
  • Female
  • HLA-DQ Antigens / genetics
  • HLA-DQ Antigens / immunology
  • HLA-DQ Antigens / metabolism*
  • Humans
  • Interferon-gamma / metabolism
  • Interleukin-10 / metabolism
  • Protein Processing, Post-Translational*
  • T-Lymphocytes / immunology*
  • T-Lymphocytes / metabolism

Substances

  • Autoantigens
  • Epitopes
  • HLA-DQ Antigens
  • Interleukin-10
  • Interferon-gamma