title: Taste cell-expressed α-glucosidase enzymes contribute to gustatory responses to disaccharides.
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 T1R-independent 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 T1R-independent (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.
authors.affiliation: Monell Chemical Senses Center, Philadelphia, PA 19104;
authors.forename: Sunil K
authors.initials: SK
authors.lastname: Sukumaran
authors.affiliation: Monell Chemical Senses Center, Philadelphia, PA 19104;
authors.forename: Karen K
authors.initials: KK
authors.lastname: Yee
authors.affiliation: Section of Oral Neuroscience, Graduate School of Dental Science, Kyushu University, Fukuoka 812-8582, Japan;
authors.forename: Shusuke
authors.initials: S
authors.lastname: Iwata
authors.affiliation: Monell Chemical Senses Center, Philadelphia, PA 19104;
authors.forename: Ramana
authors.initials: R
authors.lastname: Kotha
authors.affiliation: Department of Pediatrics, Baylor College of Medicine, Houston, TX 77030; Facultad de Ciencias Quimicas, Universidad Autonoma de San Luis Potosi, San Luis Potosi 78210, Mexico;
authors.forename: Roberto
authors.initials: R
authors.lastname: Quezada-Calvillo
authors.affiliation: Department of Pediatrics, Baylor College of Medicine, Houston, TX 77030;
authors.forename: Buford L
authors.initials: BL
authors.lastname: Nichols
authors.affiliation: Department of Chemistry, Simon Fraser University, Burnaby, BC, Canada V5A 1S6.
authors.forename: Sankar
authors.initials: S
authors.lastname: Mohan
authors.affiliation: Department of Chemistry, Simon Fraser University, Burnaby, BC, Canada V5A 1S6.
authors.forename: B Mario
authors.initials: BM
authors.lastname: Pinto
authors.affiliation: Section of Oral Neuroscience, Graduate School of Dental Science, Kyushu University, Fukuoka 812-8582, Japan;
authors.forename: Noriatsu
authors.initials: N
authors.lastname: Shigemura
authors.affiliation: Monell Chemical Senses Center, Philadelphia, PA 19104; Section of Oral Neuroscience, Graduate School of Dental Science, Kyushu University, Fukuoka 812-8582, Japan;
authors.forename: Yuzo
authors.initials: Y
authors.lastname: Ninomiya
authors.affiliation: Monell Chemical Senses Center, Philadelphia, PA 19104; rmargolskee@monell.org.
authors.forename: Robert F
authors.initials: RF
authors.lastname: Margolskee
mesh_terms: D000818:Animals; D004187:Disaccharides / Q000494:pharmacology*; D015971:Gene Expression Regulation, Enzymologic / Q000502:physiology*; D051246:Glucose Transport Proteins, Facilitative / Q000235:genetics / Q000378:metabolism; D051379:Mice; D008822:Mice, Transgenic; D043562:Receptors, G-Protein-Coupled / Q000235:genetics / Q000378:metabolism; D051269:Sodium-Glucose Transporter 1 / Q000235:genetics / Q000378:metabolism; D013649:Taste / Q000502:physiology*; D013650:Taste Buds / Q000201:enzymology*; D000520:alpha-Glucosidases / Q000096:biosynthesis* / Q000235:genetics
chemical_list: D004187:Disaccharides; D051246:Glucose Transport Proteins, Facilitative; D043562:Receptors, G-Protein-Coupled; C495675:Slc5a1 protein, mouse; D051269:Sodium-Glucose Transporter 1; C431926:taste receptors, type 1; D000520:alpha-Glucosidases
keywords: disaccharides; gustation; maltase-glucoamylase; sensory transduction; sucrase-isomaltase