Dynamics of IgM and IgG responses to the next generation of engineered Duffy binding protein II immunogen: Strain-specific and strain-transcending immune responses over a nine-year period

PLoS One. 2020 May 7;15(5):e0232786. doi: 10.1371/journal.pone.0232786. eCollection 2020.

Abstract

Background: A low proportion of P. vivax-exposed individuals acquire protective strain-transcending neutralizing IgG antibodies that are able to block the interaction between the Duffy binding protein II (DBPII) and its erythrocyte-specific invasion receptor. In a recent study, a novel surface-engineered DBPII-based vaccine termed DEKnull-2, whose antibody response target conserved DBPII epitopes, was able to induce broadly binding-inhibitory IgG antibodies (BIAbs) that inhibit P. vivax reticulocyte invasion. Toward the development of DEKnull-2 as an effective P. vivax blood-stage vaccine, we investigate the relationship between naturally acquired DBPII-specific IgM response and the profile of IgG antibodies/BIAbs activity over time.

Methodology/principal findings: A nine-year follow-up study was carried-out among long-term P. vivax-exposed Amazonian individuals and included six cross-sectional surveys at periods of high and low malaria transmission. DBPII immune responses associated with either strain-specific (Sal1, natural DBPII variant circulating in the study area) or conserved epitopes (DEKnull-2) were monitored by conventional serology (ELISA-detected IgM and IgG antibodies), with IgG BIAbs activity evaluated by functional assays (in vitro inhibition of DBPII-erythrocyte binding). The results showed a tendency of IgM antibodies toward Sal1-specific response; the profile of Sal1 over DEKnull-2 was not associated with acute malaria and sustained throughout the observation period. The low malaria incidence in two consecutive years allowed us to demonstrate that variant-specific IgG (but not IgM) antibodies waned over time, which resulted in IgG skewed to the DEKnull-2 response. A persistent DBPII-specific IgM response was not associated with the presence (or absence) of broadly neutralizing IgG antibody response.

Conclusions/significance: The current study demonstrates that long-term exposure to low and unstable levels of P. vivax transmission led to a sustained DBPII-specific IgM response against variant-specific epitopes, while sustained IgG responses are skewed to conserved epitopes. Further studies should investigate on the role of a stable and persistent IgM antibody response in the immune response mediated by DBPII.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adult
  • Antibodies, Neutralizing / immunology
  • Antibody Formation
  • Antigens, Protozoan / immunology*
  • Female
  • Humans
  • Immunoglobulin G / immunology*
  • Immunoglobulin M / immunology*
  • Malaria Vaccines / immunology
  • Malaria Vaccines / therapeutic use*
  • Malaria, Vivax / immunology
  • Malaria, Vivax / prevention & control*
  • Male
  • Middle Aged
  • Plasmodium vivax / immunology*
  • Protozoan Proteins / immunology*
  • Receptors, Cell Surface / immunology*

Substances

  • Antibodies, Neutralizing
  • Antigens, Protozoan
  • Duffy antigen binding protein, Plasmodium
  • Immunoglobulin G
  • Immunoglobulin M
  • Malaria Vaccines
  • Protozoan Proteins
  • Receptors, Cell Surface