Involvement of steroid and antioxidant pathways in spleen-mediated immunity in migratory birds

Abstract

The molecular underpinnings of the spleen-mediated immune functions during the period of heightened energetic needs in the year are not known in avian migrants. We investigated this, in Palearctic-Indian migratory male redheaded buntings, which exhibited vernal (spring) premigratory / early testicular maturation states under artificial long days. This was evidenced by increased dio2 and decreased dio3 mRNA expression in the hypothalamus, elevated levels of circulating corticosterone and testosterone, and enlarged testes in long-day-photostimulated birds, as compared to unstimulated controls under short days. The concomitant decrease in both mass and volume of the spleen, and increase in the heterophil/ lymphocyte ratio suggested the parallel innate immunity effects in photostimulated buntings. Importantly, we found increased mRNA expression of genes coding for the cytokines (il15 and il34), steroid receptors (nr3c2) and oxidative stress marker enzymes (gpx1 and sod1) in the spleen, suggesting the activation of both immune and antioxidant molecular pathways during the early photostimulated state. However, the splenic expressions of il1β, il6, tgfβ, ar and nos2 genes were not significantly different between long-day stimulated and short-day unstimulated birds. The negative correlation of plasma corticosterone levels with spleen mass further indicated a role of corticosterone in the modulation of the spleen function, probably via nr3c2 gene encoded mineralocorticoid receptors. These results suggest the activation of the spleen-mediated innate immunity in anticipation of the heightened energetic stress state of the photostimulated spring migratory/breeding period in migratory songbirds.