Targeting the Extrinsic Pathway of Hepatocyte Apoptosis Promotes Clearance of Plasmodium Liver Infection

Cell Rep. 2020 Mar 31;30(13):4343-4354.e4. doi: 10.1016/j.celrep.2020.03.032.

Abstract

Plasmodium sporozoites infect the liver and develop into exoerythrocytic merozoites that initiate blood-stage disease. The hepatocyte molecular pathways that permit or abrogate parasite replication and merozoite formation have not been thoroughly explored, and a deeper understanding may identify therapeutic strategies to mitigate malaria. Cellular inhibitor of apoptosis (cIAP) proteins regulate cell survival and are co-opted by intracellular pathogens to support development. Here, we show that cIAP1 levels are upregulated during Plasmodium liver infection and that genetic or pharmacological targeting of cIAPs using clinical-stage antagonists preferentially kills infected hepatocytes and promotes immunity. Using gene-targeted mice, the mechanism was defined as TNF-TNFR1-mediated apoptosis via caspases 3 and 8 to clear parasites. This study reveals the importance of cIAPs to Plasmodium infection and demonstrates that host-directed antimalarial drugs can eliminate liver parasites and induce immunity while likely providing a high barrier to resistance in the parasite.

Keywords: IAP antagonist; Plasmodium; SMAC mimetic; T cells; antibodies; birinapant; cIAP; immunity; inhibitor of apoptosis proteins; protection.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Administration, Oral
  • Animals
  • Apoptosis* / drug effects
  • Biological Availability
  • Caspase 3 / metabolism
  • Culicidae / parasitology
  • Dipeptides / administration & dosage
  • Dipeptides / pharmacology
  • Hepatocytes / drug effects
  • Hepatocytes / pathology*
  • Immunity / drug effects
  • Indoles / administration & dosage
  • Indoles / pharmacology
  • Inhibitor of Apoptosis Proteins / antagonists & inhibitors
  • Inhibitor of Apoptosis Proteins / metabolism
  • Life Cycle Stages / drug effects
  • Liver / parasitology*
  • Liver / pathology*
  • Malaria / immunology
  • Malaria / parasitology*
  • Malaria / pathology*
  • Plasmodium / drug effects
  • Plasmodium / growth & development
  • Plasmodium / metabolism
  • Protozoan Proteins / metabolism
  • Sporozoites / drug effects
  • Sporozoites / physiology
  • Thiazoles / pharmacology
  • Tumor Necrosis Factor-alpha / metabolism

Substances

  • Dipeptides
  • Indoles
  • Inhibitor of Apoptosis Proteins
  • LCL161
  • Protozoan Proteins
  • Thiazoles
  • Tumor Necrosis Factor-alpha
  • birinapant
  • Caspase 3