Neoself-antigens are the primary target for autoreactive T cells in human lupus

Cell. 2024 Oct 17;187(21):6071-6087.e20. doi: 10.1016/j.cell.2024.08.025. Epub 2024 Sep 13.

Abstract

Major histocompatibility complex class II (MHC-II) is the most significant genetic risk factor for systemic lupus erythematosus (SLE), but the nature of the self-antigens that trigger autoimmunity remains unclear. Unusual self-antigens, termed neoself-antigens, are presented on MHC-II in the absence of the invariant chain essential for peptide presentation. Here, we demonstrate that neoself-antigens are the primary target for autoreactive T cells clonally expanded in SLE. When neoself-antigen presentation was induced by deleting the invariant chain in adult mice, neoself-reactive T cells were clonally expanded, leading to the development of lupus-like disease. Furthermore, we found that neoself-reactive CD4+ T cells were significantly expanded in SLE patients. A high frequency of Epstein-Barr virus reactivation is a risk factor for SLE. Neoself-reactive lupus T cells were activated by Epstein-Barr-virus-reactivated cells through downregulation of the invariant chain. Together, our findings imply that neoself-antigen presentation by MHC-II plays a crucial role in the pathogenesis of SLE.

Keywords: Epstein-Bar virus; HLA class II; T cell recognition; antigen presentation; autoimmunity; immune evasion; invariant chain; self tolerance.

MeSH terms

  • Adult
  • Animals
  • Antigen Presentation*
  • Antigens, Differentiation, B-Lymphocyte / immunology
  • Antigens, Differentiation, B-Lymphocyte / metabolism
  • Autoantigens* / immunology
  • CD4-Positive T-Lymphocytes / immunology
  • Female
  • Herpesvirus 4, Human / immunology
  • Histocompatibility Antigens Class II* / immunology
  • Histocompatibility Antigens Class II* / metabolism
  • Humans
  • Lupus Erythematosus, Systemic* / immunology
  • Mice
  • Mice, Inbred C57BL
  • T-Lymphocytes / immunology

Substances

  • Autoantigens
  • Histocompatibility Antigens Class II
  • Antigens, Differentiation, B-Lymphocyte
  • invariant chain