Alloimmune activation promotes anti-cancer cytotoxicity after rat liver transplantation

PLoS One. 2014 Mar 20;9(3):e91515. doi: 10.1371/journal.pone.0091515. eCollection 2014.

Abstract

Liver transplantation for hepatocellular carcinoma (HCC) results in a specific condition where the immune response is potentially directed against both allogeneic and cancer antigens. We have investigated the level of anti-cancer immunity during allogeneic immune response. Dark Agouti-to-Lewis and Lewis-to-Lewis rat liver transplantations were performed and the recipients anti-cancer immunity was analysed at the time of alloimmune activation. The occurrence of rejection in the allogeneic recipients was confirmed by a shorter survival (p<0.01), increased liver function tests (p<0.01), the presence of signs of rejection on histology, and a donor-specific ex vivo mixed lymphocyte reaction. At the time of alloimmune activation, blood mononuclear cells of the allogeneic group demonstrated increased anti-cancer cytotoxicity (p<0.005), which was related to an increased natural killer (NK) cell frequency (p<0.05) and a higher monocyte/macrophage activation level (p<0.01). Similarly, liver NK cell anti-cancer cytotoxicity (p<0.005), and liver monocyte/macrophage activation levels (p<0.01) were also increased. The alloimmune-associated cytotoxicity was mediated through the NKG2D receptor, whose expression was increased in the rejected graft (p<0.05) and on NK cells and monocyte/macrophages. NKG2D ligands were expressed on rat HCC cells, and its inhibition prevented the alloimmune-associated cytotoxicity. Although waiting for in vivo validation, alloimmune-associated cytotoxicity after rat liver transplantation appears to be linked to increased frequencies and levels of activation of NK cells and monocyte/macrophages, and is at least in part mediated through the NKG2D receptor.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Carcinoma, Hepatocellular / immunology*
  • Carcinoma, Hepatocellular / surgery*
  • Cell Line, Tumor
  • Cytotoxicity, Immunologic*
  • Graft Rejection / immunology
  • Leukocytes, Mononuclear / pathology
  • Liver / pathology
  • Liver Neoplasms / immunology*
  • Liver Neoplasms / surgery*
  • Liver Transplantation*
  • Male
  • NK Cell Lectin-Like Receptor Subfamily K / metabolism*
  • Rats
  • Rats, Inbred Lew
  • Spleen / pathology
  • Transplantation, Homologous

Substances

  • NK Cell Lectin-Like Receptor Subfamily K

Grants and funding

This study was supported by grants from the Swiss National Science Foundation (PP00P3_139021), the Artères Foundation, the Astellas European Foundation, and the Boninchi Foundation, the Elsie and Carlos de Reuter, and the Marie-France and Francis Minkoff Foundation. Christian Toso was supported by a Professorship from the Swiss National Science Foundation (PP00P3_139021). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.