Blood Stage Malaria Disrupts Humoral Immunity to the Pre-erythrocytic Stage Circumsporozoite Protein

Cell Rep. 2016 Dec 20;17(12):3193-3205. doi: 10.1016/j.celrep.2016.11.060.

Abstract

Many current malaria vaccines target the pre-erythrocytic stage of infection in the liver. However, in malaria-endemic regions, increased blood stage exposure is associated with decreased vaccine efficacy, thereby challenging current vaccine efforts. We hypothesized that pre-erythrocytic humoral immunity is directly disrupted by blood stage infection. To investigate this possibility, we used Plasmodium-antigen tetramers to analyze B cells after infection with either late liver stage arresting parasites or wild-type parasites that progress to the blood stage. Our data demonstrate that immunoglobulin G (IgG) antibodies against the pre-erythrocytic antigen, circumsporozoite protein (CSP), are generated only in response to the attenuated, but not the wild-type, infection. Further analyses revealed that blood stage malaria inhibits CSP-specific germinal center B cell differentiation and modulates chemokine expression. This results in aberrant memory formation and the loss of a rapid secondary B cell response. These data highlight how immunization with attenuated parasites may drive optimal immunity to malaria.

Keywords: antibodies; antigen specific B cells; attenuated parasites; humoral immunity; malaria; memory B cells; plasmodium; vaccines.

Publication types

  • Research Support, N.I.H., Extramural

MeSH terms

  • Animals
  • Antigens, Protozoan / immunology
  • B-Lymphocytes / immunology
  • B-Lymphocytes / parasitology
  • Erythrocytes / immunology
  • Erythrocytes / parasitology
  • Humans
  • Immunity, Humoral*
  • Immunoglobulin G / immunology
  • Liver / immunology
  • Liver / parasitology
  • Malaria Vaccines / immunology*
  • Malaria Vaccines / therapeutic use
  • Malaria, Falciparum / genetics
  • Malaria, Falciparum / immunology*
  • Malaria, Falciparum / parasitology
  • Plasmodium falciparum / immunology*
  • Plasmodium falciparum / pathogenicity
  • Vaccination

Substances

  • Antigens, Protozoan
  • Immunoglobulin G
  • Malaria Vaccines