Modifying Enzymes Are Elicited by ER Stress, Generating Epitopes That Are Selectively Recognized by CD4+ T Cells in Patients With Type 1 Diabetes

Diabetes. 2018 Jul;67(7):1356-1368. doi: 10.2337/db17-1166. Epub 2018 Apr 13.

Abstract

In spite of tolerance mechanisms, some individuals develop T-cell-mediated autoimmunity. Posttranslational modifications that increase the affinity of epitope presentation and/or recognition represent one means through which self-tolerance mechanisms can be circumvented. We investigated T-cell recognition of peptides that correspond to modified β-cell antigens in subjects with type 1 diabetes. Modified peptides elicited enhanced proliferation by autoreactive T-cell clones. Endoplasmic reticulum (ER) stress in insulinoma cells increased cytosolic calcium and the activity of tissue transglutaminase 2 (tTG2). Furthermore, stressed human islets and insulinomas elicited effector responses from T cells specific for modified peptides, suggesting that ER stress-derived tTG2 activity generated deamidated neoepitopes that autoreactive T cells recognized. Patients with type 1 diabetes had large numbers of T cells specific for these epitopes in their peripheral blood. T cells with these specificities were also isolated from the pancreatic draining lymph nodes of cadaveric donors with established diabetes. Together, these results suggest that self-antigens are enzymatically modified in β-cells during ER stress, giving rise to modified epitopes that could serve to initiate autoimmunity or to further broaden the antigenic repertoire, activating potentially pathogenic CD4+ T cells that may not be effectively eliminated by negative selection.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't
  • Research Support, U.S. Gov't, Non-P.H.S.

MeSH terms

  • Animals
  • Antigen Presentation
  • Autoantigens / immunology
  • Autoimmunity / immunology
  • CD4-Positive T-Lymphocytes / immunology*
  • Case-Control Studies
  • Cells, Cultured
  • Diabetes Mellitus, Type 1 / immunology*
  • Diabetes Mellitus, Type 1 / metabolism
  • Endoplasmic Reticulum Stress / physiology*
  • Enzyme Activation
  • Epitopes, T-Lymphocyte / immunology
  • Epitopes, T-Lymphocyte / metabolism*
  • GTP-Binding Proteins / metabolism
  • Humans
  • Insecta
  • Insulin-Secreting Cells / immunology
  • Insulin-Secreting Cells / metabolism*
  • Protein Glutamine gamma Glutamyltransferase 2
  • Protein Processing, Post-Translational* / physiology
  • Protein-Arginine Deiminase Type 2
  • Protein-Arginine Deiminases / metabolism
  • Transglutaminases / metabolism

Substances

  • Autoantigens
  • Epitopes, T-Lymphocyte
  • TGM2 protein, human
  • Protein Glutamine gamma Glutamyltransferase 2
  • Transglutaminases
  • PADI2 protein, human
  • Protein-Arginine Deiminase Type 2
  • Protein-Arginine Deiminases
  • GTP-Binding Proteins