The antigen-presenting molecule MR1 presents microbial metabolite ligands from vitamin B2 biosynthesis to Mucosal Associated Invariant T cells (MAIT cells). While bacteria and fungi drive the MR1 biosynthesis pathway, viruses do not synthesise vitamin B metabolites and thus had not previously been implicated in MR1 expression or its antigen presentation. We have taken a multi-faceted approach to explore the relationship between herpesvirus infections and MR1 and/or MAIT cell responses.
We demonstrate that several human herpesviruses inhibit MR1 cell surface upregulation, including a potent inhibition by herpes simplex virus type 1 (HSV-1), varicella zoster virus (VZV) and human cytomegalovirus (HCMV). However, these viruses appear to employ distinct mechanisms to modulate MR1. For example, whilst HSV-1 and VZV profoundly impair total MR1 protein expression, MR1 that had already trafficked to the cell surface before infection was protected from virus-mediated targeting, yet HCMV efficiently targeted both intracellular and pre-existing surface MR1. We also show that a consequence of MR1 targeting is an impaired capacity of the MAIT TCR and/or primary MAIT cells to recognise MR1-restricted ligands during infection of target cells. Thus, virus-mediated targeting of MR1 defines an immunomodulatory strategy that functionally disrupts the MR1-MAIT cell axis.
In our related studies profiling immune reconstitution in haematopoietic stem cell transplant (HSCT) patients with the complication of HCMV reactivated infection, we identify MAIT cell levels at the initial detection of HCMV reactivation as distinguishing patients who subsequently developed low-level versus high-level HCMV reactivation. This data in the HSCT setting highlights MAIT cell levels at the first detection of reactivation as a prognostic marker that may guide clinical decisions regarding pre-emptive therapy. In summary, we provide the first identification of virus-mediated modulation of the MR1 antigen presentation pathway as well as identify impacts on MAIT cells in a clinically relevant setting of virus infection.