Multi-compartmental diversification of neutralizing antibody lineages dissected in SARS-CoV-2 spike-immunized macaques

Nat Commun. 2024 Jul 27;15(1):6338. doi: 10.1038/s41467-024-50286-0.

Abstract

The continued evolution of SARS-CoV-2 underscores the need to understand qualitative aspects of the humoral immune response elicited by spike immunization. Here, we combine monoclonal antibody (mAb) isolation with deep B cell receptor (BCR) repertoire sequencing of rhesus macaques immunized with prefusion-stabilized spike glycoprotein. Longitudinal tracing of spike-sorted B cell lineages in multiple immune compartments demonstrates increasing somatic hypermutation and broad dissemination of vaccine-elicited B cells in draining and non-draining lymphoid compartments, including the bone marrow, spleen and, most notably, periaortic lymph nodes. Phylogenetic analysis of spike-specific monoclonal antibody lineages identified through deep repertoire sequencing delineates extensive intra-clonal diversification that shaped neutralizing activity. Structural analysis of the spike in complex with a broadly neutralizing mAb provides a molecular basis for the observed differences in neutralization breadth between clonally related antibodies. Our findings highlight that immunization leads to extensive intra-clonal B cell evolution where members of the same lineage can both retain the original epitope specificity and evolve to recognize additional spike variants not previously encountered.

MeSH terms

  • Animals
  • Antibodies, Monoclonal* / immunology
  • Antibodies, Neutralizing* / immunology
  • Antibodies, Viral* / immunology
  • B-Lymphocytes* / immunology
  • COVID-19 / immunology
  • COVID-19 / virology
  • COVID-19 Vaccines / immunology
  • Epitopes / immunology
  • Humans
  • Immunization
  • Macaca mulatta*
  • Phylogeny*
  • Receptors, Antigen, B-Cell / genetics
  • Receptors, Antigen, B-Cell / immunology
  • SARS-CoV-2* / genetics
  • SARS-CoV-2* / immunology
  • Somatic Hypermutation, Immunoglobulin
  • Spike Glycoprotein, Coronavirus* / genetics
  • Spike Glycoprotein, Coronavirus* / immunology

Substances

  • Spike Glycoprotein, Coronavirus
  • Antibodies, Neutralizing
  • Antibodies, Viral
  • spike protein, SARS-CoV-2
  • Antibodies, Monoclonal
  • Epitopes
  • COVID-19 Vaccines
  • Receptors, Antigen, B-Cell