Structure of a Human Monoclonal Antibody in Complex with Outer Surface Protein C of the Lyme Disease Spirochete, Borreliella burgdorferi

J Immunol. 2024 Oct 15;213(8):1234-1243. doi: 10.4049/jimmunol.2400247.

Abstract

Lyme disease is a tick-borne, multisystem infection caused by the spirochete Borreliella burgdorferi. Although Abs have been implicated in the resolution of Lyme disease, the specific B cell epitopes targeted during human infections remain largely unknown. In this study, we characterized and defined the structural epitope of a patient-derived bactericidal monoclonal IgG (B11) against outer surface protein C (OspC), a homodimeric lipoprotein necessary for B. burgdorferi tick-mediated transmission and early-stage colonization of vertebrate hosts. High-resolution epitope mapping was accomplished through hydrogen deuterium exchange-mass spectrometry and X-ray crystallography. Structural analysis of B11 Fab-OspCA complexes revealed the B11 Fabs associated in a 1:1 stoichiometry with the lateral faces of OspCA homodimers such that the Abs are essentially positioned perpendicular to the spirochete's outer surface. B11's primary contacts reside within the membrane-proximal regions of α-helices 1 and 6 and adjacent loops 5 and 6 in one OspCA monomer. In addition, B11 spans the OspCA dimer interface, engaging opposing α-helix 1', α-helix 2', and loop 2-3' in the second OspCA monomer. The B11-OspCA structure is reminiscent of the recently solved mouse transmission blocking monoclonal IgG B5 in complex with OspCA, indicating a mode of engagement with OspC that is conserved across species. In conclusion, we provide a detailed insight into the interaction between a functional human Ab and an immunodominant Lyme disease Ag long considered an important vaccine candidate.

MeSH terms

  • Animals
  • Antibodies, Bacterial / immunology
  • Antibodies, Monoclonal* / chemistry
  • Antibodies, Monoclonal* / immunology
  • Antigens, Bacterial* / chemistry
  • Antigens, Bacterial* / immunology
  • Bacterial Outer Membrane Proteins* / chemistry
  • Bacterial Outer Membrane Proteins* / immunology
  • Borrelia burgdorferi* / immunology
  • Crystallography, X-Ray
  • Epitope Mapping / methods
  • Epitopes, B-Lymphocyte / chemistry
  • Epitopes, B-Lymphocyte / immunology
  • Humans
  • Immunoglobulin Fab Fragments / chemistry
  • Immunoglobulin Fab Fragments / immunology
  • Immunoglobulin G / immunology
  • Lyme Disease* / immunology

Substances

  • Bacterial Outer Membrane Proteins
  • Antibodies, Monoclonal
  • OspC protein
  • Antigens, Bacterial
  • Antibodies, Bacterial
  • Immunoglobulin G
  • Epitopes, B-Lymphocyte
  • Immunoglobulin Fab Fragments