Lower IgG somatic hypermutation rates during acute dengue virus infection is compatible with a germinal center-independent B cell response

Genome Med. 2016 Feb 25;8(1):23. doi: 10.1186/s13073-016-0276-1.

Abstract

Background: The study of human B cell response to dengue virus (DENV) infection is critical to understand serotype-specific protection and the cross-reactive sub-neutralizing response. Whereas the first is beneficial and thus represents the ultimate goal of vaccination, the latter has been implicated in the development of severe disease, which occurs in a small, albeit significant, fraction of secondary DENV infections. Both primary and secondary infections are associated with the production of poly-reactive and cross-reactive IgG antibodies.

Methods: To gain insight into the effect of DENV infection on the B cell repertoire, we used VH region high-throughput cDNA sequencing of the peripheral blood IgG B cell compartment of 19 individuals during the acute phase of infection. For 11 individuals, a second sample obtained 6 months later was analyzed for comparison. Probabilities of sequencing antibody secreting cells or memory B cells were estimated using second-order Monte Carlo simulation.

Results: We found that in acute disease there is an increase in IgG B cell diversity and changes in the relative use of segments IGHV1-2, IGHV1-18, and IGHV1-69. Somewhat unexpectedly, an overall low proportion of somatic hypermutated antibody genes was observed during the acute phase plasmablasts, particularly in secondary infections and those cases with more severe disease.

Conclusions: Our data are consistent with an innate-like antiviral recognition system mediated by B cells using defined germ-line coded B cell receptors, which could provide a rapid germinal center-independent antibody response during the early phase of infection. A model describing concurrent T-dependent and T-independent B cell responses in the context of DENV infection is proposed, which incorporates the selection of B cells using hypomutated IGHV segments and their potential role in poly/cross-reactivity. Its formal demonstration could lead to a definition of its potential implication in antibody-dependent enhancement, and may contribute to rational vaccine development efforts.

MeSH terms

  • Acute Disease
  • Adolescent
  • Adult
  • Amino Acid Motifs
  • B-Lymphocytes / immunology*
  • B-Lymphocytes / metabolism*
  • Cluster Analysis
  • Complementarity Determining Regions / genetics
  • Computational Biology
  • Dengue / diagnosis
  • Dengue / genetics*
  • Dengue / immunology*
  • Dengue / virology
  • Dengue Virus / classification
  • Dengue Virus / genetics
  • Dengue Virus / immunology*
  • Female
  • Gene Expression Profiling
  • Germinal Center / immunology*
  • High-Throughput Nucleotide Sequencing
  • Humans
  • Immunoglobulin G / genetics*
  • Immunoglobulin G / immunology*
  • Immunoglobulin Heavy Chains / genetics
  • Immunoglobulin Variable Region / genetics
  • Male
  • Middle Aged
  • Mutation
  • Position-Specific Scoring Matrices
  • Serogroup
  • Somatic Hypermutation, Immunoglobulin*
  • Young Adult

Substances

  • Complementarity Determining Regions
  • Immunoglobulin G
  • Immunoglobulin Heavy Chains
  • Immunoglobulin Variable Region