Taste cell-expressed α-glucosidase enzymes contribute to gustatory responses to disaccharides

Sunil K. Sukumarana, Karen K. Yeea, Shusuke Iwatab, Ramana Kothaa, Roberto Quezada-Calvillo, Buford L. Nichols, Sankar Mohan, B. Mario Pinto, Noriatsu Shigemura, Yuzo Ninomiya, Robert F. Margolskee

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33 Citations (Scopus)

Abstract

The primary sweet sensor in mammalian taste cells for sugars and noncaloric sweeteners is the heteromeric combination of type 1 taste receptors 2 and 3 (T1R2+T1R3, encoded by Tas1r2 and Tas1r3 genes). However, in the absence of T1R2+T1R3 (e.g., in Tas1r3 KO mice), animals still respond to sugars, arguing for the presence of T1Rindependent detection mechanism(s). Our previous findings that several glucose transporters (GLUTs), sodium glucose cotransporter 1 (SGLT1), and the ATP-gated K+ (KATP ) metabolic sensor are preferentially expressed in the same taste cells with T1R3 provides a potential explanation for the T1R-independent detection of sugars: sweet-responsive taste cells that respond to sugars and sweeteners may contain a T1R-dependent (T1R2+T1R3) sweet-sensing pathway for detecting sugars and noncaloric sweeteners, as well as a T1Rindependent (GLUTs, SGLT1, KATP ) pathway for detecting monosaccharides. However, the T1R-independent pathway would not explain responses to disaccharide and oligomeric sugars, such as sucrose, maltose, and maltotriose, which are not substrates for GLUTs or SGLT1. Using RT-PCR, quantitative PCR, in situ hybridization, and immunohistochemistry, we found that taste cells express multiple α-glycosidases (e.g., amylase and neutral α glucosidase C) and so-called intestinal "brush border" disaccharide-hydrolyzing enzymes (e.g., maltase-glucoamylase and sucrase-isomaltase). Treating the tongue with inhibitors of disaccharidases specifically decreased gustatory nerve responses to disaccharides, but not to monosaccharides or noncaloric sweeteners, indicating that lingual disaccharidases are functional. These taste cell-expressed enzymes may locally break down dietary disaccharides and starch hydrolysis products into monosaccharides that could serve as substrates for the T1R-independent sugar sensing pathways.

Original languageEnglish
Pages (from-to)6035-6040
Number of pages6
JournalProceedings of the National Academy of Sciences of the United States of America
Volume113
Issue number21
DOIs
Publication statusPublished - May 24 2016

All Science Journal Classification (ASJC) codes

  • General

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    Sukumarana, S. K., Yeea, K. K., Iwatab, S., Kothaa, R., Quezada-Calvillo, R., Nichols, B. L., Mohan, S., Pinto, B. M., Shigemura, N., Ninomiya, Y., & Margolskee, R. F. (2016). Taste cell-expressed α-glucosidase enzymes contribute to gustatory responses to disaccharides. Proceedings of the National Academy of Sciences of the United States of America, 113(21), 6035-6040. https://doi.org/10.1073/pnas.1520843113