Abstract
Organisms use circulating diuretic hormones to control water balance (osmolarity), thereby avoiding dehydration and managing excretion of waste products. The hormones act through G-protein-coupled receptors to activate second messenger systems that in turn control the permeability of secretory epithelia to ions like chloride. In insects, the chloride channel mediating the effects of diuretic hormones was unknown. Surprisingly, we find a pentameric, cys-loop chloride channel, a type of channel normally associated with neurotransmission, mediating hormone-induced transepithelial chloride conductance. This discovery is important because: 1) it describes an unexpected role for pentameric receptors in the membrane permeability of secretory epithelial cells, and 2) it suggests that neurotransmitter-gated ion channels may have evolved from channels involved in secretion.
Highlights
Organisms have evolved diverse mechanisms to solve the problems of osmoregulation and excretion
Both tyramine and the leucokinins stimulate diuresis by increasing net chloride transport into the lumen[1,2,5]. They appear to act through distinct G-protein coupled receptors (GPCRs) that converge on the same second messenger pathway; the diuretic action of both secretory hormones is dependent on a rise in intracellular calcium levels in stellate cells[2,6,7,8]
The holding currents of oocytes injected with secCl capped RNA (cRNA) were significantly higher than water injected controls (302 nA ± 59.6 vs. 38.9 nA ± 10.7; p < 0.002, two tailed t-test) (Fig. 1a), indicating that an open ion channel is formed in secCl -expressing oocytes
Summary
Organisms have evolved diverse mechanisms to solve the problems of osmoregulation and excretion. Much of our knowledge concerning transepithelial chloride secretion in the MTs stems from research characterizing the diuretic effects of the leucokinin neuropeptides and the biogenic amine tyramine Both tyramine and the leucokinins stimulate diuresis by increasing net chloride transport into the lumen[1,2,5]. Loss of secCl eliminates the effects of diuretic hormones and has a penetrant lethal phenotype in adults, demonstrating that secCl plays a significant role in secretion These results suggest that in Drosophila MTs, a member of the pentameric, cys-loop ligand-gated ion channel family mediates transcellular chloride secretion without direct interaction with a ligand
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