Modulation of carp (Cyprinus carpio) neutrophil functions during an infection with the haemoparasite Trypanoplasma borreli

Trypanoplasma borreli is an extracellular blood parasite of common carp (Cyprinus carpio) transmitted by fish-biting leeches. The infestation with this parasite in juvenile carp may range between 75% and 100%, especially in fish recovering from the first hibernation period. T. borreli is perfectly adapted to its prolonged survival in a cyprinid host. Elevated numbers of activated neutrophils in peripheral blood and tissues are reported during T. borreli infection, but in context of the disease, the direct reason for elevated neutrophil numbers and their role during the infection remain unclear. In this study, a quantitative transmigration system, permitting the harvest of highly pure (≥97%) neutrophil populations was applied to investigate the modulation of carp neutrophil functions during T. borreli infection. We demonstrate time-dependent kinetics of a serum-induced down-regulation of neutrophil chemotaxis and an up-regulation of ROS production during the course of infection. With highly pure neutrophil populations, we could show that this divergent alteration of neutrophil functions was neither caused by T. borreli metabolites nor by the parasite itself. Moreover, when added to highly purified neutrophils, parasite metabolites did not alter the leukotriene B4-induced neutrophil chemotaxis nor the Staphylococcus aureus-induced ROS production. We conclude that the haemoparasite T. borreli does not interact with neutrophils directly, but indirectly modulates their functions via serum factors induced by parasite interaction with other components of the immune system.