Displaced tick-parasite interactions at the host interface

Abstract

Summary: Reciprocal interactions of parasites transmitted by blood-sucking arthropod vectors have been studied primarily at the parasite–host and parasite–vector interface. The third component of this parasite triangle, the vector–host interface, has been largely ignored. Now there is growing realization that reciprocal interactions between arthropod vectors and their vertebrate hosts play a pivotal role in the survival of arthropod-borne viruses, bacteria, and protozoa. The vector–host interface is the site where the haematophagous arthropod feeds. To obtain a blood meal, the vector must overcome the host's inflammatory, haemostatic, and immune responses. This problem is greatest for ixodid ticks which may imbibe as much as 15 ml blood whilst continuously attached to their host for 10 days or more. To feed successfully, the interface between tick and host becomes a battle between the host's mechanisms for combating the tick and the tick's armoury of bioactive proteins and other chemicals which it secretes, via saliva, into the feeding lesion formed in the host's skin. Parasites entering this battlefield encounter a privileged site in their vertebrate host that has been profoundly modified by the pharmacological activities of their vector's saliva. For example, ticks suppress natural killer cells and interferons, both of which have potent antiviral activities. Not surprisingly, vector-borne parasites exploit the immunomodulated feeding site to promote their transmission and infection. Certain tick-borne viruses are so successful at this that they are transmitted from one infected tick, through the vertebrate host to a co-feeding uninfected tick, without a detectable viraemia (virus circulating in the host's blood), and with no untoward effect on the host. When such viruses do have an adverse effect on the host, they may impede their vectors' feeding. Thus important interactions between ticks and tick-borne parasites are displaced to the interface with their vertebrate host - the skin site of blood-feeding and infection.