Characterization of splenic MRC1(hi)MHCII(lo) and MRC1(lo)MHCII(hi) cells from the monocyte/macrophage lineage of White Leghorn chickens

Monocytes/macrophages, which are found in a variety of organs, maintain tissue homeostasis at a steady state and act as the first line of defence during pathogen-induced inflammation in the host. Most monocyte/macrophage lineage studies in chickens have been largely performed using cell lines, while few studies using primary cells have been conducted. In the present study, the phenotypic and functional characteristics of splenic monocyte/macrophage lineage cells during steady state and inflammatory conditions were examined. Splenic monocyte/macrophage lineage cells could be identified as MRC1(lo)MHCII(hi) and MRC1(hi)MHCII(lo) cells based on their surface expression of MRC1 and MHCII. In the steady state, MRC1(lo)MHCII(hi) cells were more frequently found among MRC1(+) cells. MRC1(lo)MHCII(hi) cells expressed a higher number of antigen-presenting molecules (MHCII, MHCI, and CD80) than MRC1(hi)MHCII(lo) cells. In contrast, MRC1(hi)MHCII(lo) cells showed better phagocytic and CCR5-dependent migratory properties than MRC1(lo)MHCII(hi) cells. Furthermore, MRC1(hi)MHCII(lo) cells infiltrated the spleen in vivo and then became MRC1(lo)MHCII(hi) cells. During lipopolysaccharide (LPS)-induced inflammatory conditions that were produced via intraperitoneal (i.p.) injection, the proportion and absolute number of MRC1(hi)MHCII(lo) cells were increased in the spleen. Uniquely, inflammation induced the downregulation of MHCII expression in MRC1(hi)MHCII(lo) cells. The major source of inflammatory cytokines (IL-1β, IL-6, and IL-12) was MRC1(lo)MHCII(hi) cells. Furthermore, MRC1(hi)MHCII(lo) cells showed greater bactericidal activity than MRC1(lo)MHCII(hi) cells during LPS-induced inflammation. Collectively, these results suggest that two subsets of monocyte/macrophage lineage cells exist in the chicken spleen that have functional differences.