ERAP1 and ERAP2 Haplotypes Influence Suboptimal HLA-B*27:05-Restricted Anti-Viral CD8+ T Cell Responses Cross-Reactive to Self-Epitopes

Int J Mol Sci. 2023 Aug 28;24(17):13335. doi: 10.3390/ijms241713335.

Abstract

The human leukocyte antigen (HLA)-B*27 family of alleles is strongly associated with ankylosing spondylitis (AS), a chronic inflammatory disorder affecting the axial and peripheral joints, yet some HLA-B*27 variants not associated with AS have been shown. Since no major differences in the ligandome of associated compared to not-associated alleles have emerged, a plausible hypothesis is that the quantity rather than the quality of the presented epitopes makes the difference. In addition, the Endoplasmic Reticulum AminoPeptidases (ERAPs) 1 and 2, playing a crucial role in shaping the HLA class I epitopes, act as strong AS susceptibility factors, suggesting that an altered peptidome might be responsible for the activation of pathogenic CD8+ T cells. In this context, we have previously singled out a B*27:05-restricted CD8+ T cell response against pEBNA3A (RPPIFIRRL), an EBV peptide lacking the B*27 classic binding motif. Here, we show that a specific ERAP1/2 haplotype negatively correlates with such response in B*27:05 subjects. Moreover, we prove that the B*27:05 allele successfully presents peptides with the same suboptimal N-terminal RP motif, including the self-peptide, pDYNEIN (RPPIFGDFL). Overall, this study underscores the cooperation between the HLA-B*27 and ERAP1/2 allelic variants in defining CD8+ T cell reactivity to suboptimal viral and self-B*27 peptides and prompts further investigation of the B*27:05 peptidome composition.

Keywords: CD8+ T cells; Endoplasmic Reticulum AminoPeptidase (ERAP)1 and ERAP2 haplotypes; ankylosing spondylitis; anti-viral immunity; antigen processing and presentation; human leukocyte antigen (HLA)-B*27; peptides.

MeSH terms

  • Aminopeptidases / genetics
  • CD8-Positive T-Lymphocytes
  • Epitopes
  • Genes, MHC Class I*
  • HLA-B Antigens / genetics
  • Haplotypes
  • Humans
  • Minor Histocompatibility Antigens / genetics
  • Spondylitis, Ankylosing* / genetics

Substances

  • HLA-B Antigens
  • Epitopes
  • ERAP1 protein, human
  • Aminopeptidases
  • Minor Histocompatibility Antigens
  • ERAP2 protein, human