The Peptidome of Behçet's Disease-Associated HLA-B*51:01 Includes Two Subpeptidomes Differentially Shaped by Endoplasmic Reticulum Aminopeptidase 1

Arthritis Rheumatol. 2016 Feb;68(2):505-15. doi: 10.1002/art.39430.

Abstract

Objective: To characterize the peptidome of the Behçet's disease-associated HLA-B*51:01 allotype as well as the differential features of major peptide subsets and their distinct endoplasmic reticulum aminopeptidase 1 (ERAP-1)-mediated processing.

Methods: The endogenous B*51:01-bound peptidome was characterized from 721.221 transfectant cells, after affinity chromatography and acid extraction, by tandem mass spectrometry. Recombinant ERAP-1 variants were used to digest synthetic B*51:01 ligands. HLA and transporter associated with antigen processing (TAP) binding affinities of peptide ligands were calculated with well-established algorithms. ERAP-1 and ERAP-2 from 721.221 cells were characterized by genomic sequencing and Western blotting.

Results: The B*51:01 peptidome consisted of 29.5% octamers, 61.7% nonamers, 4.8% decamers, and 4.0% longer peptides. The major peptide motif consisted of Pro and Ala at position 2, aliphatic/aromatic position 3 residues, and Val and Ile at the C-terminal position. The ligands with Pro or Ala at position 2 constituted 2 distinct subpeptidomes. Peptides with Pro at position 2 showed higher affinity for B*51:01 and lower affinity for TAP than those with Ala at position 2. Most important, both peptide subsets differed drastically in the susceptibility of their position 1 residues to ERAP-1, revealing a distinct influence of this enzyme on both subpeptidomes, which may alter their balance, affecting the global affinity of B*51:01-peptide complexes.

Conclusion: ERAP-1 has a significant influence on the B*51:01 peptidome and its affinity. This influence is based on very distinct effects on the 2 subpeptidomes, whereby only peptides in the subpeptidome with Ala at position 2 are extensively destroyed, except when their position 1 residues are ERAP-1 resistant. This pattern provides a mechanism for the epistatic association of ERAP-1 and B*51:01 in Behçet's disease.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • ATP-Binding Cassette Transporters / metabolism
  • Aminopeptidases / genetics*
  • Aminopeptidases / metabolism
  • Behcet Syndrome / metabolism*
  • Cell Line
  • Chromatography, Affinity
  • Genotype
  • HLA-B51 Antigen / metabolism*
  • Humans
  • Minor Histocompatibility Antigens
  • Peptides / metabolism*
  • Polymorphism, Single Nucleotide
  • Tandem Mass Spectrometry

Substances

  • ATP-Binding Cassette Transporters
  • HLA-B51 Antigen
  • Minor Histocompatibility Antigens
  • Peptides
  • transporter associated with antigen processing (TAP)
  • Aminopeptidases
  • ERAP1 protein, human
  • ERAP2 protein, human