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Intestinal absorption of D-fructose isomers, D-allulose, D-sorbose and D-tagatose, via glucose transporter type 5 (GLUT5) but not sodium-dependent glucose cotransporter 1 (SGLT1) in rats

Published online by Cambridge University Press:  03 May 2023

Kunihiro Kishida*
Affiliation:
Department of Science and Technology on Food Safety, Kindai University, 930 Nishimitani, Kinokawa, Wakayama 649-6493, Japan
Tetsuo Iida
Affiliation:
Research and Development, Matsutani Chemical Industry Company, Limited, 5-3 Kita-Itami, Itami, Hyogo 664-8508, Japan
Takako Yamada
Affiliation:
Research and Development, Matsutani Chemical Industry Company, Limited, 5-3 Kita-Itami, Itami, Hyogo 664-8508, Japan
Yukiyasu Toyoda
Affiliation:
Department of Pathobiochemistry, Faculty of Pharmacy, Meijo University, 150 Yagotoyama, Tempaku-ku, Nagoya, Aichi 468-8503, Japan
*
*Corresponding author: Kunihiro Kishida, email kishida@waka.kindai.ac.jp

Abstract

D-allulose, D-sorbose and D-tagatose are D-fructose isomers that are called rare sugars. These rare sugars have been studied intensively in terms of biological production and food application as well as physiological effects. There are limited papers with regard to the transporters mediating the intestinal absorption of these rare sugars. We examined whether these rare sugars are absorbed via sodium-dependent glucose cotransporter 1 (SGLT1) as well as via GLUT type 5 (GLUT5) using rats. High-fructose diet fed rats, which express more intestinal GLUT5, exhibited significantly higher peripheral concentrations, Cmax and AUC0–180 min when D-allulose, D-sorbose and D-tagatose were orally administrated. KGA-2727, a selective SGLT1 inhibitor, did not affect the peripheral and portal vein concentrations and pharmacokinetic parameters of these rare sugars. The results suggest that D-allulose, D-sorbose and D-tagatose are likely transported via GLUT5 but not SGLT1 in rat small intestine.

Type
Research Article
Copyright
© The Author(s), 2023. Published by Cambridge University Press on behalf of The Nutrition Society

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References

International Society of Rare Sugars (ISRS) (2002) Definition of Rare Sugars. https://www.isrs.kagawa-u.ac.jp/definition.html (accessed January 2023).Google Scholar
Chen, Z, Chen, J, Zhang, W, et al. (2018) Recent research on the physiological functions, applications, and biotechnological production of D-allose. Appl Microbiol Biotechnol 102, 42694278.CrossRefGoogle ScholarPubMed
Guerrero-Wyss, M, Duran Aguero, S & Angarita Davila, L (2018) D-tagatose is a promising sweetener to control glycaemia: a new functional food. Biomed Res Int 2018, 8718053.CrossRefGoogle ScholarPubMed
Gullapalli, P, Takata, G, Poonperm, W, et al. (2007) Bioproduction of D-psicose from allitol with Enterobacter aerogenes IK7: a new frontier in rare ketose production. Biosci Biotechnol Biochem 71, 30483054.10.1271/bbb.70450CrossRefGoogle ScholarPubMed
Hoshikawa, H, Kamitori, K, Indo, K, et al. (2018) Combined treatment with D-allose, docetaxel and radiation inhibits the tumor growth in an in vivo model of head and neck cancer. Oncol lett 15, 34223428.Google Scholar
Hossain, A, Yamaguchi, F, Matsuo, T, et al. (2015) Rare sugar D-allulose: potential role and therapeutic monitoring in maintaining obesity and type 2 diabetes mellitus. Pharmacol Ther 155, 4959.10.1016/j.pharmthera.2015.08.004CrossRefGoogle ScholarPubMed
Itoh, K, Mizuno, S, Hama, S, et al. (2015) Beneficial effects of supplementation of the rare sugar ‘D-allulose’ Against Hepatic Steatosis and Severe Obesity in Lep(ob)/Lep(ob) Mice. J Food Sci 80, H16191626.CrossRefGoogle Scholar
Iwasaki, Y, Sendo, M, Dezaki, K, et al. (2018) GLP-1 release and vagal afferent activation mediate the beneficial metabolic and chronotherapeutic effects of D-allulose. Nat Commun 9, 113.10.1038/s41467-017-02488-yCrossRefGoogle ScholarPubMed
Jayamuthunagai, J, Gautam, P, Srisowmeya, G, et al. (2017) Biocatalytic production of D-tagatose: a potential rare sugar with versatile applications. Crit Rev Food Sci Nutr 57, 34303437.CrossRefGoogle ScholarPubMed
Kimura, T, Kanasaki, A, H, ayashi, N, et al. (2017) D-Allulose enhances postprandial fat oxidation in healthy humans. Nutrition 43–44, 1620.CrossRefGoogle ScholarPubMed
Mooradian, AD, Smith, M & Tokuda, M (2017) The role of artificial and natural sweeteners in reducing the consumption of table sugar: a narrative review. Clin Nutr ESPEN 18, 18.CrossRefGoogle ScholarPubMed
Nagata, Y, Mizuta, N, Kanasaki, A, et al. (2018) Rare sugars, D-allulose, D-tagatose and D-sorbose, differently modulate lipid metabolism in rats. J Sci Food Agric 98, 20202026.CrossRefGoogle ScholarPubMed
Oku, T, Murata-Takenoshita, Y, Yamazaki, Y, et al. (2014) D-sorbose inhibits disaccharidase activity and demonstrates suppressive action on postprandial blood levels of glucose and insulin in the rat. Nutr Res 34, 961967.CrossRefGoogle ScholarPubMed
Roy, S, Chikkerur, J, Roy, SC, et al. (2018) Tagatose as a potential nutraceutical: production, properties, biological roles, and applications. J Food Sci 83, 26992709.CrossRefGoogle ScholarPubMed
Shinohara, N, Nakamura, T, Abe, Y, et al. (2016) D-Allose attenuates overexpression of inflammatory cytokines after cerebral ischemia/reperfusion injury in gerbil. J Stroke Cerebrovasc Dis: Offic J Natl Stroke Assoc 25, 21842188.CrossRefGoogle ScholarPubMed
Shintani, T, Sakoguchi, H, Yoshihara, A, et al. (2017) D-Allulose, a stereoisomer of D-fructose, extends Caenorhabditis elegans lifespan through a dietary restriction mechanism: a new candidate dietary restriction mimetic. Biochem Biophys Res Commun 493, 15281533.10.1016/j.bbrc.2017.09.147CrossRefGoogle ScholarPubMed
Yamada, T, Hayashi, N, Iida, T, et al. (2014) Dietary D-sorbose decreases serum insulin levels in growing Sprague-Dawley rats. J Nutr Sci Vitaminol 60, 297299.CrossRefGoogle ScholarPubMed
Levin, GV (2002) Tagatose, the new GRAS sweetener and health product. J Med Food 5, 2336.CrossRefGoogle ScholarPubMed
Armstrong, LM, Luecke, KJ & Bell, LN (2009) Consumer evaluation of bakery product flavour as affected by incorporating the prebiotic tagatose. Int J Food Sci Technol 44, 815819.CrossRefGoogle Scholar
Jürkenbeck, K, Haarhoff, T, Spiller, A, et al. (2022) Does allulose appeal to consumers? Results from a discrete choice experiment in Germany. Nutrients 14, 3350.CrossRefGoogle ScholarPubMed
Daniel, H, Hauner, H, Hornef, M, et al. (2021) Allulose in human diet: the knowns and the unknowns. Br J Nutr 128, 172178.CrossRefGoogle ScholarPubMed
Matsuo, T, Tanaka, T, Hashiguchi, M, et al. (2003) Metabolic effects of D-psicose in rats: studies on faecal and urinary excretion and caecal fermentation. Asia Pac J Clin Nutr 12, 225231.Google ScholarPubMed
Tsukamoto, I, Hossain, A, Yamaguchi, F, et al. (2014) Intestinal absorption, organ distribution, and urinary excretion of the rare sugar D-psicose. Drug Devel Ther 8, 19551964.Google ScholarPubMed
Saunders, JP, Zehner, LR & Levin, GV (1999) Disposition of D-(U-14C)tagatose in the rat. Regul Toxicol Pharmacol: RTP 29, S4656.CrossRefGoogle ScholarPubMed
Normen, L, Laerke, HN, Jensen, BB, et al. (2001) Small-bowel absorption of D-tagatose and related effects on carbohydrate digestibility: an ileostomy study. Am J Clin Nutr 73, 105110.CrossRefGoogle ScholarPubMed
Kitagawa, M, Tanaka, M, Yoshikawa, Y, et al. (2018) Evaluation of absorption and fermentability of D-mannose, D-sorbose, and D-allose in humans. J Jpn Assoc for Dietary Fiber Res 22, 7582.Google Scholar
Iga, Y & Matsuo, T (2010) D-allose metabolism in rats. Nippon Eiyo Shokuryo Gakkaishi 63, 1719.10.4327/jsnfs.63.17CrossRefGoogle Scholar
Kishida, K, Martinez, G, Iida, T, et al. (2019) D-allulose is a substrate of glucose transporter type 5 (GLUT5) in the small intestine. Food Chem 277, 604608.CrossRefGoogle ScholarPubMed
Kishida, K, Iida, T, Yamada, T, et al. (2021) D-Allose is absorbed via sodium-dependent glucose cotransporter 1 (SGLT1) in the rat small intestine. Metab Open 11, 100112.CrossRefGoogle ScholarPubMed
Shibazaki, T, Tomae, M, Ishikawa-Takemura, Y, et al. (2012) KGA-2727, a novel selective inhibitor of a high-affinity sodium glucose cotransporter (SGLT1), exhibits antidiabetic efficacy in rodent models. J Pharmacol Exp Therap 342, 288296.10.1124/jpet.112.193045CrossRefGoogle ScholarPubMed
Ferraris, RP, Choe, JY & Patel, CR (2018) Intestinal absorption of fructose. Annu Rev Nutr 38, 4167.CrossRefGoogle ScholarPubMed
Patel, C, Douard, V, Yu, S, et al. (2015) Metabolism, and endosomal trafficking-dependent regulation of intestinal fructose absorption. FASEB J: Offic Publ Fed Am Soc Exp Biol 29, 40464058.CrossRefGoogle ScholarPubMed
Iida, T, Hayashi, N, Yamada, T, et al. (2010) Failure of D-psicose absorbed in the small intestine to metabolize into energy and its low large intestinal fermentability in humans. Metab Clin Exp 59, 206214.10.1016/j.metabol.2009.07.018CrossRefGoogle ScholarPubMed
Matsuo, T, Suzuki, H, Hashiguchi, M, et al. (2002) D-psicose is a rare sugar that provides no energy to growing rats. J Nutr Sci Vitaminol 48, 7780.CrossRefGoogle ScholarPubMed
Burns, JJ, Mosbach, EH, Schulenberg, S, et al. (1955) Studies on the incorporation of C14 administered as L-sorbose into L-ascorbic acid and D-glucose in rats. J Biol Chem 214, 507514.CrossRefGoogle ScholarPubMed
Rognstad, R (1975) Gluconeogenesis from D-tagatose by isolated rat and hamster liver cells. FEBS Lett 52, 292294.CrossRefGoogle ScholarPubMed
Rognstad, R (1982) Pathway of gluconeogenesis from tagatose in rat hepatocytes. Arch Biochem Biophys 218, 488491.CrossRefGoogle ScholarPubMed
Wright, EM, Loo, DD & Hirayama, BA (2011) Biology of human sodium glucose transporters. Physiol Rev 91, 733794.CrossRefGoogle ScholarPubMed
Blaschek, W (2017) Natural products as lead compounds for Sodium Glucose Cotransporter (SGLT) inhibitors. Planta Med 83, 985993.Google ScholarPubMed
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