Water-specific and aquaglyceroporins in ticks: Lessons from functional studies in feeding ticks

Adult female ticks imbibe a tremendous volume of blood increasing their body weight 100-fold and returning about 1/3 this volume back into the host via the saliva.  We investigated the role of a water-specific aquaporin (tick-APQ1) and glyceraquaporin (tick-GLP) in feeding ticks. Tick-AQP1 contained the typical NPA-motif, transported only water when expressed in Xenopus oocytes and was most abundantly expressed in the salivary glands specifically restricted to f-cells within type III acini.  When tick-AQP1 expression was abolished by gene-knockdown, feeding ticks had greatly decreased body weight (50%) and increased haemolymph and saliva osmolarity. Overall, tick-AQP1 appeared a critical, but orthodox, AQP involved in the water balance of feeding ticks.  In contrast, tick-GLP contained an NPI-motif rather than the usual NPA-motif and was ubiquitously expressed at a relatively low level in all tissues.  Tick-GLP transported water, glycerol, sorbitol and urea in Xenopus oocytes.  However, tick-GLP ceased to transport anything other than water if the NPI-motif was mutated to the more usual NPA-motif.  When tick-GLP expression was abolished by gene-knockdown, feeding ticks exhibited only a moderate reduction (15%) in body weight but 185% increase in haemolymph urea concentration.  This is the first demonstration of a role for an aquaporin in urea transport in any animal, not just an invertebrate.  Further, the evidence of a ureotelic mechanism of nitrogenous waste handling in arthropods with high protein diets might open potential Achilles’ heel targets for controlling blood feeding vectors.