Unexpected similarity of intestinal sugar absorption by SGLT1 and apical GLUT2 in an insect (Aphidius ervi,Hymenoptera) and mammals

Abstract

Sugars are critical substrates for insect metabolism, but little is known about the transporters and epithelial routes that ensure their constant supply from dietary resources. We have characterized glucose and fructose uptakes across the apical and basolateral membranes of the isolated larval midgut of the aphid parasitoid Aphidius ervi. The uptake of radiolabeled glucose at the basal side of the epithelium was almost suppressed by 200 microM cytochalasin B, uninhibited by phlorizin, and showed the following decreasing rank of specificity for the tested substrates: glucose > glucosamine > fructose, with no recognition of galactose. These functional properties well agree with the expression of GLUT2-like transporters in this membrane. When the apical surface of the epithelium was also exposed to the labeled medium, a cation-dependent glucose uptake, inhibited by 10 microM phlorizin and by an excess of galactose, was detected suggesting the presence in the apical membrane of a cation-dependent cotransporter. Radiolabeled fructose uptakes were only partially inhibited by cytochalasin B. SGLT1-like and GLUT5-like transporters were detected in the apical membranes of the epithelial cell by immunocytochemical experiments. These results, along with the presence of GLUT2-like transporters both in the apical and basolateral cell membranes of the midgut, as we recently demonstrated, allow us to conclude that the model for sugar transepithelial transport in A. ervi midgut appears to be unexpectedly similar to that recently proposed for sugar intestinal absorption in mammals.

Transepitheliald-glucose andd-fructose transport across the American lobster,Homarus americanus, intestine

“…The presence of an SGLT1-like glucose transporter on the mucosal membrane of the lobster intestine, as shown by the inhibition of glucose transport in the presence of phloridizin (Fig.3A), has previously been reported in mammals (Drozodowski and Thomson, 2006;Helliwell and Kellett, 2002;Turk et al, 1994;Turk and Wright, 1997), parasitic wasp larvae (Caccia et al, 2007), blue crabs (Chu, 1986), freshwater prawns (Ahearn and Maginniss, 1977) and a variety of other vertebrates and invertebrates. Although mammalian and crustacean intestines appear to have similar mucosal glucose and fructose transporters, SGLT1 and GLUT5 respectively, the kinetic constants for these transporters in these organisms differ.…”

“…The results revealed the localization of SGLT1 and GLUT5 on the apical membrane (Caccia et al, 2007). GLUT2 was shown to be present on the basolateral side of the gut and, in the presence of high concentrations of sugars, GLUT2 was inserted into the apical side of the membrane to maximize uptake of the sugars (Caccia et al, 2007). The findings by these authors are important because they are the only known nonvertebrate eukaryote study that describes in detail the mechanism for carrier-mediated transport of sugars across an invertebrate epithelium, and they also support the evolutionary conservation of sugar transporters in eukaryotic organisms.…”

“…Recently, a detailed investigation of transepithelial D-glucose and D-fructose transport across invertebrate epithelial cells, and how transporter members of the SLC5 and SLC2 gene families might be involved in these processes, was reported for the larval midgut of the parasitic wasp A. ervi (Caccia et al, 2007). This study used the combination of radiolabeled hexoses and immunocytochemical localization methods to define the sugar transport systems present on both brush border and basolateral membranes of this gastrointestinal epithelium.…”

“…In a study conducted on the midgut of the wasp larva Aphidius ervi, apical and basolateral fluxes of D-glucose and D-fructose, immunocytochemistry and western blot analysis were used to determine the characteristics and localization of sugar transport proteins in midgut epithelial plasma membranes (Caccia et al, 2007). The results revealed the localization of SGLT1 and GLUT5 on the apical membrane (Caccia et al, 2007).…”

“…In a study conducted on the midgut of the wasp larva Aphidius ervi, apical and basolateral fluxes of D-glucose and D-fructose, immunocytochemistry and western blot analysis were used to determine the characteristics and localization of sugar transport proteins in midgut epithelial plasma membranes (Caccia et al, 2007). The results revealed the localization of SGLT1 and GLUT5 on the apical membrane (Caccia et al, 2007). GLUT2 was shown to be present on the basolateral side of the gut and, in the presence of high concentrations of sugars, GLUT2 was inserted into the apical side of the membrane to maximize uptake of the sugars (Caccia et al, 2007).…”