A dynamic paracellular pathway serves diuresis in mosquito Malpighian tubules

Abstract

Female mosquitoes gorge on vertebrate blood, a rich nutrient source for developing eggs. But gorging meals increase the risk of predation. Mosquitoes are quick to reduce the flight payload with a potent diuresis. Diuretic peptides of the insect kinin family induce a tenfold-reduction in the paracellular resistance of Malpighian tubules and increase the paracellular permeation of Cl−, the counterion of the transepithelial secretion of Na+ and K+. As a result, the transepithelial secretion of NaCl and KCl and water increases. Insect kinins signal to the opening of the paracellular pathway via G protein-coupled receptors and the elevation of intracellular [Ca2+], which leads to the reorganization of the cytoskeleton associated with the septate junction. The reorganization may affect the septate junctional proteins that control the barrier and permselectivity properties of the paracellular pathway. The proteins involved in the embryonic formation of the septate junction and in epithelial polarization are largely known for ectodermal epithelia, but the proteins that form and mediate the dynamic functions of the septate junction in Malpighian tubules remain to be determined.

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

“…Aquaporins 1, 2 and 4 are down regulated by 3 h after the blood meal, corresponding to the time by which excretion of the bulk of the blood meal-derived water has been excreted (Drake et al, 2010). Furthermore, the mosquito releases diuretic peptides from the brain such as aedeskinin and mosquito naturietic peptide into the hemolymph immediately after feeding; these then stimulate the fluid-secreting Malpighian tubules of the mosquito (Beyenbach, 2012). Through the activation of G-protein coupled receptors and the release of intracellular Ca 2+ stores, the paracellular resistance of the Malpighian tubules decreases tenfold leading to a "leaky epithelium" that allows a dramatic increase in the transepithelial secretion of NaCl, KCl and water which are then eliminated by the mosquito (Beyebach, 2012).…”

“…More than 60% of the amino acids are oxidized to carbon dioxide to provide the energy needed for egg production (Briegel, 1985;Zhoe et al, 2004). The mosquito doubles its body weight in less than two minutes during feeding, resulting in an array of different physiological stresses on the mosquito (Beyenbach, 2012).…”

Shaping up for action

“…It has been hypothesized that modification to scaffold and cytoskeletal proteins results in the "unzipping" of the septate junction paracellular strands to bring about increased paracellular Clconductance. 84 In support of this, actin, adducin and actin-depolymerising factors are mobilised after kinin stimulation. [84][85][86] Similarly, movement of water occurs through both transcellular and paracellular routes (Fig.…”

“…84 In support of this, actin, adducin and actin-depolymerising factors are mobilised after kinin stimulation. [84][85][86] Similarly, movement of water occurs through both transcellular and paracellular routes (Fig. 3A).…”

Copper II - polar amino acid complexes: toxicity to bacteria and larvae of Aedes aegypti

“…L-glutamate (excitatory) and γ-amino butyric acid (inhibitor) are neurotransmitters that control the permeability of chloride ions (Cl -) and the change in this interaction may lead to greater permeability to Cl -ions, causing nervous hyperexcitation (Beyenbach 2012), which is metabolically important because it causes an increase in the metabolic activity of oxidative stress induced by the presence of transition metals. Thus, the control of immature stages of insects can be proposed by the action of metallic complexes in the digestive system and neuromuscular junction (glutaminergic action).…”