Multiple functions of Na/K-ATPase in dopamine-induced salivation of the Blacklegged tick, Ixodes scapularis.

Donghun Kim,Joshua Urban,Yoonseong Park,Daniel L Boyle

doi:10.1038/srep21047

Abstract

Control of salivary secretion in ticks involves autocrine dopamine activating two dopamine receptors: D1 and Invertebrate-specific D1-like dopamine receptors. In this study, we investigated Na/K-ATPase as an important component of the secretory process. Immunoreactivity for Na/K-ATPase revealed basal infolding of lamellate cells in type-I, abluminal interstitial (epithelial) cells in type-II, and labyrinth-like infolding structures opening towards the lumen in type-III acini. Ouabain (10 μmol l−1), a specific inhibitor of Na/K-ATPase, abolished dopamine-induced salivary secretion by suppressing fluid transport in type III acini. At 1 μmol l−1, ouabain, the secreted saliva was hyperosmotic. This suggests that ouabain also inhibits an ion resorptive function of Na/K-ATPase in the type I acini. Dopamine/ouabain were not involved in activation of protein secretion, while dopamine-induced saliva contained constitutively basal level of protein. We hypothesize that the dopamine-dependent primary saliva formation, mediated by Na/K-ATPase in type III and type II acini, is followed by a dopamine-independent resorptive function of Na/K-ATPase in type I acini located in the proximal end of the salivary duct.

Highlights

Control of salivary secretion in ticks involves autocrine dopamine activating two dopamine receptors: D1 and Invertebrate-specific D1-like dopamine receptors
Phylogenetic analysis using the neighbor joining method showed that the single copy Na/K-ATPases in arthropods are all clustered in a monophyletic group (Fig. 1D)
This study revealed a number of unique features of tick salivary glands

Summary

Introduction

Control of salivary secretion in ticks involves autocrine dopamine activating two dopamine receptors: D1 and Invertebrate-specific D1-like dopamine receptors. Ouabain (10 μmol l−1), a specific inhibitor of Na/K-ATPase, abolished dopamine-induced salivary secretion by suppressing fluid transport in type III acini. The salivary secretion at the very early stage of feeding contains immunosuppressive and other bioactive components that promote the successful establishment of the feeding lesion[9,10,11,12]; these are secreted by the granular cells of the type II and type III acini. Another important function of the tick SG is the excretion of excess ions and water from the blood meal (mainly in type III acini). Silencing of the Na/K-ATPase gene via RNA interference demonstrated the importance of Na/K-ATPase to blood feeding and www.nature.com/scientificreports/

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Conclusion