Aquaporin water channel AgAQP1 in the malaria vector mosquito Anopheles gambiae during blood feeding and humidity adaptation

Abstract

Altered patterns of malaria endemicity reflect, in part, changes in feeding behavior and climate adaptation of mosquito vectors. Aquaporin (AQP) water channels are found throughout nature and confer high-capacity water flow through cell membranes. The genome of the major malaria vector mosquito Anopheles gambiae contains at least seven putative AQP sequences. Anticipating that transmembrane water movements are important during the life cycle of A. gambiae , we identified and characterized the A. gambiae aquaporin 1 (AgAQP1) protein that is homologous to AQPs known in humans, Drosophila , and sap-sucking insects. When expressed in Xenopus laevis oocytes, AgAQP1 transports water but not glycerol. Similar to mammalian AQPs, water permeation of AgAQP1 is inhibited by HgCl 2 and tetraethylammonium, with Tyr185 conferring tetraethylammonium sensitivity. AgAQP1 is more highly expressed in adult female A. gambiae mosquitoes than in males. Expression is high in gut, ovaries, and Malpighian tubules where immunofluorescence microscopy reveals that AgAQP1 resides in stellate cells but not principal cells. AgAQP1 expression is up-regulated in fat body and ovary by blood feeding but not by sugar feeding, and it is reduced by exposure to a dehydrating environment (42% relative humidity). RNA interference reduces AgAQP1 mRNA and protein levels. In a desiccating environment (<20% relative humidity), mosquitoes with reduced AgAQP1 protein survive significantly longer than controls. These studies support a role for AgAQP1 in water homeostasis during blood feeding and humidity adaptation of A. gambiae , a major mosquito vector of human malaria in sub-Saharan Africa.

Impact of trehalose transporter knockdown onAnopheles gambiaestress adaptation and susceptibility toPlasmodium falciparuminfection

“…Four hundred nanograms of dsRNA was injected into the thorax of mosquitoes, and the mosquitoes were cultivated at 17°C and 80% relative humidity to recover until the desiccation assay as described (3) or the heat assay in this paragraph. Both assays were repeated three times with similar results.…”

“…Mosquitoes adapt to environmental changes by adjusting expression levels of certain genes (2); however, most protective mechanisms apparently remain unknown. Recently, we characterized an aquaporin water channel from A. gambiae (AgAQP1) that is important for water homeostasis, because reduced expression protected against dehydration (3). Since water loss has profound effects on mosquito physiology, we investigated other candidate genes that may protect against environmental stress and may affect transmission of P. falciparum.…”

A comprehensive transcriptomic view of renal function in the malaria vector, Anopheles gambiae

“…The data further show that the larval and adult tubules use the same subset of V-ATPase genes to encode the plasma membrane V-ATPase (Table 2). Similarly, the Na + , K + ATPase (Patrick and Gill, 2002), the aquaporin DRIP (Liu et al, 2011) and the apical exchanger (Rheault et al, 2007;Xiang et al, 2011;Xiang et al, 2012b) have all been described in mosquito tubule; these array data provide a more comprehensive survey of which genes in a particular family show highly enriched expression in the tubule.…”

Identification and characterisation of functional aquaporin water channel (Anomala cuprea DRIP) in a coleopteran insect

“…The physiological role of specific AQPs in insect osmoregulation has been determined in liquid feeders, such as the green leafhopper (Le Cahérec et al, 1996), the buffalo fly (Elvin et al, 1999), two mosquitoes (Pietrantonio et al, 2000;Liu et al, 2011), the pea aphid (Shakesby et al, 2009) and the whitefly (Mathew et al, 2011). These Group 1 AQPs are localised to the alimentary tract (midgut and hindgut) and Malpighian tubules (MTs; insect kidney) for osmoregulation in diuresis and excretion through several transporters and channels across each epithelium.…”