Transport mechanisms of diuresis in Malpighian tubules of insects

Abstract

SUMMARYWe have studied Malpighian tubules of Aedes aegypti using a variety of methods: Ramsay fluid secretion assay, electron probe analysis of secreted fluid, in vitro microperfusion and two-electrode voltage clamp. Collectively, these methods have allowed us to elucidate transepithelial transport mechanisms under control conditions and in the presence of diuretic peptides. Mosquito natriuretic peptide (MNP), a corticotropin-releasing factor (CRF)-like diuretic peptide, selectively increases transepithelial secretion of NaCl and water, meeting the NaCl loads of the blood meal. The intracellular messenger of MNP is cAMP, which increases the Na+ conductance and activates the Na+/K+/2Cl--cotransporter in the basolateral membrane of principal cells. Leucokinin non-selectively increases transepithelial NaCl and KCl secretion, which may deal with hemolymph volume expansions or reduce the flight pay load upon eclosion from the aquatic habitat. The non-selective NaCl and KCl diuresis stems from the increase in septate junctional Cl- conductance activated by leucokinin using Ca2+ as second messenger. Fundamental to diuretic mechanisms are powerful epithelial transport mechanisms in the distal segment of the Malpighian tubules, where transepithelial secretion rates can exceed the capacity of mammalian glomerular kidneys in the renal turnover of the extracellular fluid compartment. In conjunction with powerful epithelial transport mechanisms driven by the V-type H+-ATPase, diuretic hormones enable hematophagous and probably also phytophagous insects to deal with enormous dietary loads, thereby contributing to the evolutionary success of insects.

Transport of H+, Na+ and K+ across the posterior midgut of blood-fed mosquitoes (Aedes aegypti)

“…In addition, little is known of the effects of diuretic factors on ion transport across the posterior midgut. Mosquito natriuretic factor and leucokinin both stimulate fluid secretion by the Malpighian tubules (Beyenbach, 2003), and it would be of interest to determine the effects of these peptides on Na + transport across the posterior midgut. Letters denote significant differences between time points (ANOVA; P<0.05).…”

“…Although the secretion of fluid and ions during diuresis have been studied extensively (reviewed by Beyenbach, 2003), relatively little is known of the patterns and mechanisms of inorganic ion transport across the posterior midgut during and after diuresis. Immunohistochemical studies have revealed the locations of the Na + /K + -ATPase, the V-type H + -ATPase in the adult midgut (Patrick et al, 2006), but the roles of these transporters in movement of ions across the midgut after the blood meal have not been determined.…”

Cell signalling mechanisms for insect stress tolerance

“…As insect Malpighian tubules are fluid-secreting tissues, tubule ion transport pathways have been extensively mapped (Beyenbach, 2003;O'Donnell et al, 2003;Spring et al, 2009;Wieczorek et al, 2009), with tubules from D. melanogaster holding the distinction of being the fastest fluid-transporting epithelia known in biology (Maddrell, 2009). However, much more remains to be discovered, including neuroendocrine control of ion transport and fluid secretion (Coast, 2007).…”

Drinking a hot blood meal elicits a protective heat shock response in mosquitoes

“…Imbibing a huge blood meal also quickly generates osmotic stress that requires an efficient excretory system for rapid removal of excess water (2)(3)(4)(5). However, one overlooked challenge of feeding on mammalian blood is the high temperature of the blood that rushes into the gut.…”