MR1 is a major histocompatibility complex (MHC) class I-like molecule that presents microbial metabolites derived from the riboflavin biosynthesis pathway to mucosal-associated invariant T (MAIT) cells. Numerous studies now report that MR1 can bind a plethora of other small molecules of microbial, environmental, synthetic, or endogenous cellular origin, some of which may be recognised by MAIT cells or other MR1-reactive T cells in the context of infection, allergy, autoimmunity, or cancer. Many of these known or proposed MR1 ligands exist as structurally related families of chemical adducts with highly reactive cellular dicarbonyls such as glyoxal, methylglyoxal, and malondialdehyde (MDA). Using a selection of newly described MR1 ligands of such nature, we generated MR1 tetramers to identify and extensively characterise MAIT and other MR1-reactive T cell responses in the blood from healthy human donors.
We found that adducts of MDA were presented by MR1 and recognised by two distinct populations of T cells: namely, MAIT cells bearing unique T cell receptors (TCRs) and non-MAIT, predominantly CD8+, T cells bearing diverse TCRs. These MR1-reactive T cells were present at a low frequency in blood but were detected in almost all healthy donors after enrichment. MAIT and non-MAIT MR1-reactive T cells exhibited varying degrees of antigen-dependent as well as allomorph-dependent MR1 reactivity and produced T helper (Th)1 type cytokines upon stimulation. Polyclonal MR1-reactive T cells from healthy donors displayed potent cytotoxicity to transformed and tumour-derived cell lines. Our findings demonstrate that MR1-reactive T cells are common in healthy donors and that these cells bear TCRs with the collective capacity to recognise and elicit immunity to MR1 furnishing structurally distinct molecules from a burgeoning diversity of sources.