Characterizing Intestinal Glucose Absorption in Mammalian Pig and Aquatic Species Tilapia and Trout

Abstract

Glucose absorption along the intestine primarily occurs through sodium-dependent glucose transporters (SGLTs). Recently, it has been suggested that glucose transport across the brush-border membrane (BBM, or apical side of epithelial cells) can also occur through sodium-independent/facilitative glucose transporters (GLUTs) in mammals. Here, the Ussing chamber was used to characterize sodium-dependent and sodium-independent glucose transport systems across ex-vivo intestinal segments in the mammalian pig, and the aquatic species tilapia and trout. In our first study, electrogenic sodium-dependent glucose transport in tilapia demonstrated a homogeneous high-affinity, high-capacity (Ha/Hc) transport system across the proximal intestine, mid-intestine, and hindgut segments, associated with transporters from the solute carrier 5A (SLC5A) family. In contrast, trout demonstrated a heterogeneous glucose transport system with a high-affinity, low-capacity (Ha/Lc) in the pyloric caeca, a super-high-affinity, low-capacity (sHa/Lc) in the midgut, and a low-affinity, low-capacity (La/Lc) in the hindgut, associated with different expressions of SLC5A transporters in each segment. Additionally, fish were different from mammals in demonstrating hindgut sodium-dependent glucose absorption. In our second study, we found that sodium-dependent glucose and galactose transport along the porcine jejunum and ileum followed sigmoidal/Hill kinetics. This strongly suggested that each segment had multiple transporter involvement. The transport systems in the jejunum demonstrated a Ha/super-low-capacity (sLc) for glucose and a La/Lc for galactose. In contrast, the ileum demonstrated a Ha/super-high-capacity (sHc) glucose transport system, and a La/Hc galactose transport system. In support of this, different SLC5A transporters were associated with the kinetics in each segment. Finally, the absence of monosaccharide transport in the colon was supported with pharmacological data and low expression of all SLC5A genes. Our last study characterized total tissue glucose flux in tilapia, trout, and pig. We demonstrated a Ha/Hc system in tilapia, a Ha/Lc system in trout, and a La/Lc system in the pig. The overall La system in the pig, with differences in pharmacological inhibition and gene expression in comparison to the aquatic species, revealed a different mechanism of glucose transport in the pig. Interestingly, our results revealed the possible involvement of AQPs in tilapia and pig to total tissue glucose absorption. Overall, our results in each study highlighted the fact that aquatic species have divergently adapted mechanisms for glucose absorption differing from the mammalian pig, which may have evolved to meet their individual needs.