Plasmodium berghei infection in mice induces liver injury by an IL-12- and toll-like receptor/myeloid differentiation factor 88-dependent mechanism

J Immunol. 2001 Nov 15;167(10):5928-34. doi: 10.4049/jimmunol.167.10.5928.

Abstract

Malaria, caused by infection with Plasmodium spp., is a life cycle-specific disease that includes liver injury at the erythrocyte stage of the parasite. In this study, we have investigated the mechanisms underlying Plasmodium berghei-induced liver injury, which is characterized by the presence of apoptotic and necrotic hepatocytes and dense infiltration of lymphocytes. Although both IL-12 and IL-18 serum levels were elevated after infection, IL-12-deficient, but not IL-18-deficient, mice were resistant to liver injury induced by P. berghei. Neither elevation of serum IL-12 levels nor liver injury was observed in mice deficient in myeloid differentiation factor 88 (MyD88), an adaptor molecule shared by Toll-like receptors (TLRs). These results demonstrated a requirement of the TLR-MyD88 pathway for induction of IL-12 production during P. berghei infection. Hepatic lymphocytes from P. berghei-infected wild-type mice lysed hepatocytes from both uninfected and infected mice. The hepatocytotoxic action of these cells was blocked by a perforin inhibitor but not by a neutralizing anti-Fas ligand Ab and was up-regulated by IL-12. Surprisingly, these cells killed hepatocytes in an MHC-unrestricted manner. However, CD1d-deficient mice that lack CD1d-restricted NK T cells, were susceptible to liver injury induced by P. berghei. Collectively, our results indicate that the liver injury induced by P. berghei infection of mice induces activation of the TLR-MyD88 signaling pathway which results in IL-12 production and activation of the perforin-dependent cytotoxic activities of MHC-unrestricted hepatic lymphocytes.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adaptor Proteins, Signal Transducing
  • Animals
  • Antigens, CD1 / analysis
  • Antigens, CD1d
  • Antigens, Differentiation / genetics
  • Antigens, Differentiation / physiology*
  • Cytotoxicity Tests, Immunologic
  • Drosophila Proteins*
  • Fas Ligand Protein
  • Female
  • Hepatitis, Animal / etiology
  • Hepatitis, Animal / parasitology*
  • Hepatitis, Animal / pathology
  • Interleukin-12 / genetics
  • Interleukin-12 / physiology*
  • Interleukin-18 / genetics
  • Interleukin-18 / physiology
  • Killer Cells, Natural / immunology
  • Liver / pathology
  • Malaria / etiology*
  • Malaria / pathology
  • Membrane Glycoproteins / genetics
  • Membrane Glycoproteins / physiology*
  • Mice
  • Mice, Knockout
  • Myeloid Differentiation Factor 88
  • Perforin
  • Plasmodium berghei*
  • Pore Forming Cytotoxic Proteins
  • Receptors, Cell Surface / physiology*
  • Receptors, Immunologic*
  • T-Lymphocyte Subsets / immunology
  • Toll-Like Receptors
  • fas Receptor / physiology

Substances

  • Adaptor Proteins, Signal Transducing
  • Antigens, CD1
  • Antigens, CD1d
  • Antigens, Differentiation
  • Drosophila Proteins
  • Fas Ligand Protein
  • Fasl protein, mouse
  • Interleukin-18
  • Membrane Glycoproteins
  • Myd88 protein, mouse
  • Myeloid Differentiation Factor 88
  • Pore Forming Cytotoxic Proteins
  • Receptors, Cell Surface
  • Receptors, Immunologic
  • Toll-Like Receptors
  • fas Receptor
  • Perforin
  • Interleukin-12