Aaron Fleming, Karen Neish, Rafael Di Marco-Barros, David A Posner, Colin Y C Lee, Andrew Stewart, Zewen Kelvin Tuong, Miles Bremridge, Ana Peñalver, Mia Cabantous, Nathan Richoz, Anais Portet, Katherine Harcourt, Eleanor Gillman, Tammie Tao Min Sow, Tetsuo Hasegawa, David Ruano-Gallego, Gad Frankel, David Withers, Simon Clare, Menna R Clatworthy
The meninges form the border between the brain and periphery and house a rich network of immune cells. Here we show that gastrointestinal challenges (intracellular or extracellular bacteria and parasites) reshape the nature of CD4+ T cells in the dura mater, the outer meningeal layer, changing the dominant polarization states to T helper (TH) 1, TH17 and TH2 cells, respectively, with differing cytokine profiles. This occurs via CXCR6-CXCL16-dependent migration of gut-activated CD4+ T cells to the central nervous system, where they establish long-lived memory populations around the dural venous sinuses, within dural lymphoid aggregates and in the brain. Functionally, these orally primed dural CD4+ T were capable of rapid, antigen-specific recall responses, proliferating and producing cytokines upon intravenous rechallenge. Our findings reveal a direct link between intestinal and dural immunity, enabling the central nervous system borders to acquire immunological memory of gut microorganisms, a major source of bloodborne pathogens capable of reaching the brain via fenestrated dural vasculature.