MAIT cells are protective against liver cancer, a major cause of cancer death worldwide, in murine models. However, in human cancer patients, MAIT cells are rendered dysfunctional for unclear reasons. Here, we aim to unravel the molecular mechanisms of MAIT cell cytotoxicity and dysfunction within the tumour microenvironment in human cancer patients with the aim to identify novel, MAIT cell-targeted anti-cancer strategies.
MAIT cells were isolated from human liver tissue and peripheral blood. Primary MAIT cells were co-cultured with various liver cancer cell lines and primary human hepatocytes in vitro. MAIT cell phenotype and function were analysed by multi-colour flow cytometry. MAIT cell cytotoxicity was tested by real-time viability assays using xCelligence.
Here, we uncover a so far unrecognised, direct cytotoxic capacity of human MAIT cells against hepatocellular carcinoma (HCC) cells employing an in vitro co-culture system. Importantly, activated MAIT cells selectively killed HCC cells but not primary hepatocytes. T cell receptor-mediated activation of MAIT cells was indispensable for MAIT cell cytotoxicity, which was, however, independent of MR1 signalling. Mechanistically, MAIT cell cytotoxicity required signalling via death receptors of the tumour necrosis factor superfamily and effector cytokines secreted by MAIT cells. In human HCC patients, MAIT cells are systemically reduced in frequency and excluded from HCC tumour tissue. Moreover, tumour-educated MAIT cells express a dysfunctional phenotype, which was directly induced by HCC cells in a cell contact-dependent manner, or by metabolites in the tumour microenvironment. Importantly, such MAIT dysfunction resulted in poorer clinical outcomes for patients with HCC. MAIT cell cytotoxicity could be enhanced by targeting the death receptor – cytokine axis we have identified.
Our results demonstrate a novel, direct cytotoxic capacity of human MAIT cells against HCC cells, which is dependent on death receptor signalling and MAIT cell cytokines. These findings suggest that enhancing the anti-tumour potential of MAIT cells could be harnessed to improve current immunotherapeutic strategies.