Voltage-gated ion channels as novel regulators of epithelial ion transport in the osmoregulatory organs of insects

Abstract

Voltage-gated ion channels (VGICs) respond to changes in membrane potential (V_m) and typically exhibit fast kinetic properties. They play an important role in signal detection and propagation in excitable tissues. In contrast, the role of VGICs in non-excitable tissues like epithelia is less studied and less clear. Studies in epithelia of vertebrates and invertebrates demonstrate wide expression of VGICs in epithelia of animals. Recently, VGICs have emerged as regulators of ion transport in the Malpighian tubules (MTs) and other osmoregulatory organs of insects. This mini-review aims to concisely summarize which VGICs have been implicated in the regulation of ion transport in the osmoregulatory epithelia of insects to date, and highlight select groups for further study. We have also speculated on the roles VGICs may potentially play in regulating processes connected directly to ion transport in insects (e.g., acid-base balance, desiccation, thermal tolerance). This review is not meant to be exhaustive but should rather serve as a thought-provoking collection of select existing highlights on VGICs, and to emphasize how understudied this mechanism of ion transport regulation is in insect epithelia.

Keywords: Malpighian tubules; excretion; ion transport; salt and water balance; voltage-gated ion channels.

Figure 1

(A) Malpighian tubules (MTs) are blind outpouchings between the midgut and the hindgut of an insect - they secrete fluid by secreting ions into the lumen, and allowing water to follow by osmosis, with a paracellular junction leak component. Structure and functional adaptation depends on the insect clade. (B) In the larval lepidopterans, the distal end of each tubule is embedded into the rectal complex (in longitudinal section, dashed blue line, top panel). Each embedded tubule connects to the ‘free’ (unattached) region, suspended in the hemolymph and closely juxtaposed to the gut. Larvae have two options as a source of ions and water for secreting fluid in their MTs. The reabsorptive option (in purple) sources ions and water from the gut by way of the blind embedded tubules when the caterpillars are well fed. Some ions reabsorbed from the gut are transferred into the hemolymph across the unattached MTs. The secretory option (in red) sources ions and water from the larva’s hemolymph, when dietary ions and/or water are unavailable or are in short supply (e.g., postprandially or during molting). (C) The switchover between reabsorption and secretion takes as little as 10 min.