Article


The innate immune system recognizes and regulates major histocompatibility complex class I (MHCI) expression on MHCIlow tumor cells

Bent Rubin, Joëlle Riond, Laetitia Courtiade, Nicolas Roullet and Jean-Edouard Gairin

Institut de Sciences et Technologies du Médicament de Toulouse (ISTMT), UMR-2587, CNRS-Pierre Fabre, Toulouse, France

Communicated by: RD Schreiber

Keywords: in vitro, spleen cells, cultured tumor cells, MHCI, innate immunity


Abstract

Tumor cells and the immune system play a lethal "pas de deux" during tumor development. However, it is not clear which role the innate immune system plays in these interactions. We studied the interaction of normal spleen cells (NSCs) with tumor cells expressing low levels of MHCI on the cell surface. This interaction induces increased MHCI expression on the MHCIlow tumor cells by a cell-cell contact-dependent, IFN-γ-mediated mechanism. The effector cells responsible for the increased IFN-γ production were identified as CD4+ CD1d-independent NKT cells, NK1.1+ NK cells and CD4+ CD11c+ DCs. The possible three cell collaboration is not activated by MHCIhigh tumor cells or normal fibroblasts. Kinetic experiments showed that the increase in IFN-γ production induced by MHCIlow tumor cells happens in two consecutive waves, an early peak around 12 hours, followed by a second more important peak around day 2-3. Thus, we propose that CD4+ CD1d-independent NKT cells are activated by the MHCIlow tumor cells, they release IFN-γ stimulating DCs to produce IL-12, which in turn activates NK cells to produce large amounts of IFN-γ. The recognition mechanism used by the CD4+ CD1d-independent non-classical NKT cells is unknown. Monoclonal antibody (mAb) blocking experiments using antibodies against either activating or inhibitory receptors or co-receptors on NKT/NK cells gave no conclusive results. Moreover, NSCs from either normal or MHCII-/- mice augmented MHCI expression on MHCIlow tumors, excluding a significant role of CD4-MHCII interactions in the system. Hence the initial recognition mechanism in this system still awaits further experimentation.