Characterization of anti-EBNA-1 antibodies and exploration of their molecular mimicry potential in an EBV-infected Sjögren's syndrome patient

Biochem Biophys Res Commun. 2024 Nov 26:735:150839. doi: 10.1016/j.bbrc.2024.150839. Epub 2024 Oct 16.

Abstract

There is a potential link between autoimmune diseases and Epstein-Barr virus (EBV) infections, with EBV playing a substantial role in the onset of Sjögren's syndrome (SjS). Some EBV proteins could mimic host self-antigens post-infection, leading to molecular mimicry. This similarity may cause the immune system to attack its tissues mistakenly. Among the various proteins associated with EBV, nuclear antigen 1 (EBNA-1) is essential for the latent replication of infected cells and is prevalent in all EBV-related diseases. In the study, single-chain variable fragment (scFv) antibodies targeting EBNA-1 were isolated using phage display technology from a primary SjS patient who also had a chronic active EBV infection. The specific clones were enriched after panning, and the binding activity of selected scFvs targeting EBNA-1 was confirmed. Sequence analysis indicated that the scFvs exhibiting positive signals could be grouped into five clones, all of which used homologous heavy chain V regions derived from germline Vh4-39, and two types of light chain V regions stemming from germline Vλ1-44 and Vλ3-15. These scFvs were found to exhibit a high degree of somatic mutations, likely indicative of antigen selection. Of the scFvs, P1-3 demonstrated the strongest binding affinity to EBNA-1, exhibiting a determined value of 7.3 x 10-8 M, and showed cross-reactivity to the SjS associated La/SSB self-antigen. The experimental results combined with AlphaFold 3 predictions revealed a potential epitope for scFv P1-3 binding to EBNA-1. Additionally, scFv P1-3 could also cross-bind to the modeled structure of La/SSB. We inferred a possible structural correlation between EBNA-1 and La/SSB involving an X2AX6PG epitope motif. This research contributes to our understanding of the structural basis of the interactions between antibodies and EBNA-1, shedding light on the VH and VL gene usage of anti-EBNA-1 antibodies in EBV-infected SjS patients and the potential origins of autoantibodies.

MeSH terms

  • Amino Acid Sequence
  • Antibodies, Viral / immunology
  • Epitopes / immunology
  • Epstein-Barr Virus Infections* / immunology
  • Epstein-Barr Virus Infections* / virology
  • Epstein-Barr Virus Nuclear Antigens* / immunology
  • Herpesvirus 4, Human* / immunology
  • Humans
  • Molecular Mimicry* / immunology
  • Single-Chain Antibodies* / chemistry
  • Single-Chain Antibodies* / genetics
  • Single-Chain Antibodies* / immunology
  • Sjogren's Syndrome* / immunology
  • Sjogren's Syndrome* / virology

Substances

  • Epstein-Barr Virus Nuclear Antigens
  • EBV-encoded nuclear antigen 1
  • Single-Chain Antibodies
  • Epitopes
  • Antibodies, Viral