Control of Plasmodium falciparum erythrocytic cycle: γδ T cells target the red blood cell-invasive merozoites

Blood. 2011 Dec 22;118(26):6952-62. doi: 10.1182/blood-2011-08-376111. Epub 2011 Nov 1.

Abstract

The control of Plasmodium falciparum erythrocytic parasite density is essential for protection against malaria, because it prevents pathogenesis and progression toward severe disease. P falciparum blood-stage parasite cultures are inhibited by human Vγ9Vδ2 γδ T cells, but the underlying mechanism remains poorly understood. Here, we show that both intraerythrocytic parasites and the extracellular red blood cell-invasive merozoites specifically activate Vγ9Vδ2 T cells in a γδ T cell receptor-dependent manner and trigger their degranulation. In contrast, the γδ T cell-mediated antiparasitic activity only targets the extracellular merozoites. Using perforin-deficient and granulysin-silenced T-cell lines, we demonstrate that granulysin is essential for the in vitro antiplasmodial process, whereas perforin is dispensable. Patients infected with P falciparum exhibited elevated granulysin plasma levels associated with high levels of granulysin-expressing Vδ2(+) T cells endowed with parasite-specific degranulation capacity. This indicates in vivo activation of Vγ9Vδ2 T cells along with granulysin triggering and discharge during primary acute falciparum malaria. Altogether, this work identifies Vγ9Vδ2 T cells as unconventional immune effectors targeting the red blood cell-invasive extracellular P falciparum merozoites and opens novel perspectives for immune interventions harnessing the antiparasitic activity of Vγ9Vδ2 T cells to control parasite density in malaria patients.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Antigens, Differentiation, T-Lymphocyte / genetics
  • Antigens, Differentiation, T-Lymphocyte / immunology
  • Antigens, Differentiation, T-Lymphocyte / metabolism
  • Blotting, Western
  • Cells, Cultured
  • Erythrocytes / immunology*
  • Erythrocytes / metabolism
  • Erythrocytes / parasitology
  • Flow Cytometry
  • Host-Parasite Interactions / immunology
  • Humans
  • Immunophenotyping
  • Life Cycle Stages / immunology
  • Lymphocyte Activation / immunology
  • Lysosomal-Associated Membrane Protein 1 / immunology
  • Lysosomal-Associated Membrane Protein 1 / metabolism
  • Malaria, Falciparum / genetics
  • Malaria, Falciparum / immunology
  • Malaria, Falciparum / metabolism
  • Merozoites / growth & development
  • Merozoites / immunology
  • Merozoites / physiology
  • Mutation
  • Perforin / genetics
  • Perforin / immunology
  • Perforin / metabolism
  • Plasmodium falciparum / growth & development
  • Plasmodium falciparum / immunology*
  • Plasmodium falciparum / physiology
  • RNA Interference
  • Receptors, Antigen, T-Cell, gamma-delta / immunology*
  • Receptors, Antigen, T-Cell, gamma-delta / metabolism
  • Schizonts / growth & development
  • Schizonts / immunology
  • Schizonts / physiology
  • T-Lymphocytes / immunology*
  • T-Lymphocytes / metabolism

Substances

  • Antigens, Differentiation, T-Lymphocyte
  • GNLY protein, human
  • Lysosomal-Associated Membrane Protein 1
  • Receptors, Antigen, T-Cell, gamma-delta
  • Perforin