A novel member of the trehalose transporter family functions as an h(+)-dependent trehalose transporter in the reabsorption of trehalose in malpighian tubules.

Shingo Kikuta,Yuka Hagiwara-Komoda,Takahiro Kikawada,Hiroaki Noda

doi:10.3389/fphys.2012.00290

Abstract

In insects, Malpighian tubules are functionally analogous to mammalian kidneys in that they not only are essential to excrete waste molecules into the lumen but also are responsible for the reabsorption of indispensable molecules, such as sugars, from the lumen to the principal cells. Among sugars, the disaccharide trehalose is highly important to insects because it is the main hemolymph sugar to serve as a source of energy and carbon. The trehalose transporter TRET1 participates in the transfer of newly synthesized trehalose from the fat body across the cellular membrane into the hemolymph. Although transport proteins must play a pivotal role in the reabsorption of trehalose in Malpighian tubules, the molecular context underlying this process remains obscure. Previously, we identified a Tret1 homolog (Nlst8) that is expressed principally in the Malpighian tubules of the brown planthopper (BPH). Here, we used the Xenopus oocyte expression system to show that NlST8 exerts trehalose transport activity that is elevated under low pH conditions. These functional assays indicate that Nlst8 encodes a proton-dependent trehalose transporter (H-TRET1). To examine the involvement of Nlst8 in trehalose reabsorption, we analyzed the sugar composition of honeydew by using BPH with RNAi gene silencing. Trehalose was detected in the honeydew as waste excreted from Nlst8-dsRNA-injected BPH under hyperglycemic conditions. However, trehalose was not expelled from GFP-dsRNA-injected BPH even under hyperglycemic conditions. We conclude that NlST8 could participate in trehalose reabsorption driven by a H+ gradient from the lumen to the principal cells of the Malpighian tubules.

Highlights

Excretory organs, kidneys in vertebrates and the Malpighian tubules in invertebrates, are essential to discharge waste, such as small molecules and excess salt, into the renal lumen
In mammals, sodium-glucose co-transporter 2 (SGLT2), which is expressed in the apical membrane of kidney cells facing the lumen, has a pivotal role in glucose reabsorption driven by electrochemical membrane potentials (Wright, 2001)
No fluorescence was detected in a sham control (Figure 1C). These results indicate that Nlst8 encodes a membrane-bound protein

Summary

Introduction

Kidneys in vertebrates and the Malpighian tubules in invertebrates, are essential to discharge waste, such as small molecules and excess salt, into the renal lumen. For small molecules in particular, this excretion step occurs through nonselective filtration, which means that the molecules required by living organisms must be retrieved from the waste. Another function of excretory organs is to reabsorb indispensable molecules, including sugars, amino acids, and water, via dedicated transporters located in the cellular membrane. In mammals, sodium-glucose co-transporter 2 (SGLT2), which is expressed in the apical membrane of kidney cells facing the lumen, has a pivotal role in glucose reabsorption driven by electrochemical membrane potentials (Wright, 2001). Trehalose was thought to be reabsorbed from the lumen to the principal cells of the tubules (Knowles, 1975; Jarial and Kelly-Worden, 2011), the molecular basis of this process has remained unknown

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