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Resistant maltodextrin promotes fasting glucagon-like peptide-1 secretion and production together with glucose tolerance in rats

  • Tohru Hira (a1), Asuka Ikee (a2), Yuka Kishimoto (a3), Sumiko Kanahori (a3) and Hiroshi Hara (a1)...

Abstract

Glucagon-like peptide-1 (GLP-1), which is produced and released from enteroendocrine L cells, plays pivotal roles in postprandial glycaemia. The ingestion of resistant maltodextrin (RMD), a water-soluble non-digestible saccharide, improves the glycaemic response. In the present study, we examined whether the continuous feeding of RMD to rats affected GLP-1 levels and glycaemic control. Male Sprague–Dawley rats (6 weeks of age) were fed an American Institute of Nutrition (AIN)-93G-based diet containing either cellulose (5 %) as a control, RMD (2·5 or 5 %), or fructo-oligosaccharides (FOS, 2·5 or 5 %) for 7 weeks. During the test period, an intraperitoneal glucose tolerance test (IPGTT) was performed after 6 weeks. Fasting GLP-1 levels were significantly higher in the 5 % RMD group than in the control group after 6 weeks. The IPGTT results showed that the glycaemic response was lower in the 5 % RMD group than in the control group. Lower caecal pH, higher caecal tissue and content weights were observed in the RMD and FOS groups. Proglucagon mRNA levels were increased in the caecum and colon of both RMD and FOS groups, whereas caecal GLP-1 content was increased in the 5 % RMD group. In addition, a 1 h RMD exposure induced GLP-1 secretion in an enteroendocrine L-cell model, and single oral administration of RMD increased plasma GLP-1 levels in conscious rats. The present study demonstrates that continuous ingestion of RMD increased GLP-1 secretion and production in normal rats, which could be stimulated by its direct and indirect (enhanced gut fermentation) effects on GLP-1-producing cells, and contribute to improving glucose tolerance.

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Corresponding author

* Corresponding author: T. Hira, fax +81 11 706 2811, email hira@chem.agr.hokudai.ac.jp

References

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1 Cho, YM, Fujita, Y & Kieffer, TJ (2014) Glucagon-like peptide-1: glucose homeostasis and beyond. Annu Rev Physiol 76, 535559.
2 Kim, YO & Schuppan, D (2012) When GLP-1 hits the liver: a novel approach for insulin resistance and NASH. Am J Physiol Gastrointest Liver Physiol 302, G759G761.
3 Drucker, DJ, Dritselis, A & Kirkpatrick, P (2010) Liraglutide. Nat Rev Drug Discov 9, 267268.
4 Madsbad, S, Kielgast, U, Asmar, M, et al. (2011) An overview of once-weekly glucagon-like peptide-1 receptor agonists – available efficacy and safety data and perspectives for the future. Diabetes Obes Metab 13, 394407.
5 Yazbeck, R, Howarth, GS & Abbott, CA (2009) Dipeptidyl peptidase inhibitors, an emerging drug class for inflammatory disease? Trends Pharmacol Sci 30, 600607.
6 Mochida, T, Hira, T & Hara, H (2010) The corn protein, zein hydrolysate, administered into the ileum attenuates hyperglycemia via its dual action on glucagon-like peptide-1 secretion and dipeptidyl peptidase-IV activity in rats. Endocrinology 151, 30953104.
7 Higuchi, N, Hira, T, Yamada, N, et al. (2013) Oral administration of corn zein hydrolysate stimulates GLP-1 and GIP secretion and improves glucose tolerance in male normal rats and Goto–Kakizaki rats. Endocrinology 154, 30893098.
8 Jakubowicz, D, Froy, O, Ahrén, B, et al. (2014) Incretin, insulinotropic and glucose-lowering effects of whey protein pre-load in type 2 diabetes: a randomised clinical trial. Diabetologia 57, 18071811.
9 Reimann, F, Williams, L, da Silva Xavier, G, et al. (2004) Glutamine potently stimulates glucagon-like peptide-1 secretion from GLUTag cells. Diabetologia 47, 15921601.
10 Greenfield, JR, Farooqi, IS, Keogh, JM, et al. (2009) Oral glutamine increases circulating glucagon-like peptide 1, glucagon, and insulin concentrations in lean, obese, and type 2 diabetic subjects. Am J Clin Nutr 89, 106113.
11 Baer, DJ, Stote, KS, Henderson, T, et al. (2014) The metabolizable energy of dietary resistant maltodextrin is variable and alters fecal microbiota composition in adult men. J Nutr 144, 10231029.
12 Livesey, G & Tagami, H (2009) Interventions to lower the glycemic response to carbohydrate foods with a low-viscosity fiber (resistant maltodextrin): meta-analysis of randomized controlled trials. Am J Clin Nutr 89, 114125.
13 Hashizume, C, Kishimoto, Y, Kanahori, S, et al. (2012) Improvement effect of resistant maltodextrin in humans with metabolic syndrome by continuous administration. J Nutr Sci Vitaminol (Tokyo) 58, 423430.
14 Kishimoto, Y, Oga, H, Tagami, H, et al. (2007) Suppressive effect of resistant maltodextrin on postprandial blood triacylglycerol elevation. Eur J Nutr 46, 133138.
15 Miyazato, S, Nakagawa, C, Kishimoto, Y, et al. (2010) Promotive effects of resistant maltodextrin on apparent absorption of calcium, magnesium, iron and zinc in rats. Eur J Nutr 49, 165171.
16 Fastinger, ND, Karr-Lilienthal, LK, Spears, JK, et al. (2008) A novel resistant maltodextrin alters gastrointestinal tolerance factors, fecal characteristics, and fecal microbiota in healthy adult humans. J Am Coll Nutr 27, 356366.
17 Cani, PD, Dewever, C & Delzenne, NM (2004) Inulin-type fructans modulate gastrointestinal peptides involved in appetite regulation (glucagon-like peptide-1 and ghrelin) in rats. Br J Nutr 92, 521526.
18 Cani, PD, Daubioul, CA, Reusens, B, et al. (2005) Involvement of endogenous glucagon-like peptide-1 (7–36) amide on glycaemia-lowering effect of oligofructose in streptozotocin-treated rats. J Endocrinol 185, 457465.
19 Delzenne, NM, Cani, PD, Daubioul, C, et al. (2005) Impact of inulin and oligofructose on gastrointestinal peptides. Br J Nutr 93, Suppl. 1, S157S161.
20 Reimer, RA & Russell, JC (2008) Glucose tolerance, lipids, and GLP-1 secretion in JCR:LA-cp rats fed a high protein fiber diet. Obesity (Silver Spring) 16, 4046.
21 Zhou, J, Martin, RJ, Tulley, RT, et al. (2008) Dietary resistant starch upregulates total GLP-1 and PYY in a sustained day-long manner through fermentation in rodents. Am J Physiol Endocrinol Metab 295, E1160E1166.
22 Tolhurst, G, Heffron, H, Lam, YS, et al. (2012) Short-chain fatty acids stimulate glucagon-like peptide-1 secretion via the G-protein-coupled receptor FFAR2. Diabetes 61, 364371.
23 Reeves, PG (1997) Components of the AIN-93 diets as improvements in the AIN-76A diet. J Nutr 127, 838S841S.
24 Cacho, J, Sevillano, J, de Castro, J, et al. (2008) Validation of simple indexes to assess insulin sensitivity during pregnancy in Wistar and Sprague–Dawley rats. Am J Physiol Endocrinol Metab 295, E1269E1276.
25 Cani, PD, Hoste, S, Guiot, Y, et al. (2007) Dietary non-digestible carbohydrates promote L-cell differentiation in the proximal colon of rats. Br J Nutr 98, 3237.
26 Iwaya, H, Lee, JS, Yamagishi, S, et al. (2012) The delay in the development of experimental colitis from isomaltosyloligosaccharides in rats is dependent on the degree of polymerization. PLOS ONE 7, e50658.
27 Hira, T, Mochida, T, Miyashita, K, et al. (2009) GLP-1 secretion is enhanced directly in the ileum but indirectly in the duodenum by a newly identified potent stimulator, zein hydrolysate, in rats. Am J Physiol Gastrointest Liver Physiol 297, G663G671.
28 Muramatsu, M, Hira, T, Mitsunaga, A, et al. (2014) Activation of the gut calcium-sensing receptor by peptide agonists reduces rapid elevation of plasma glucose in response to oral glucose load in rats. Am J Physiol Gastrointest Liver Physiol 306, G1099G1107.
29 Moritoh, Y, Takeuchi, K & Hazama, M (2009) Chronic administration of voglibose, an α-glucosidase inhibitor, increases active glucagon-like peptide-1 levels by increasing its secretion and decreasing dipeptidyl peptidase-4 activity in ob/ob mice. J Pharmacol Exp Ther 329, 669676.
30 Parker, HE, Adriaenssens, A, Rogers, G, et al. (2012) Predominant role of active versus facilitative glucose transport for glucagon-like peptide-1 secretion. Diabetologia 55, 24452455.
31 Gribble, FM, Williams, L, Simpson, AK, et al. (2003) A novel glucose-sensing mechanism contributing to glucagon-like peptide-1 secretion from the GLUTag cell line. Diabetes 52, 11471154.
32 Hira, T, Muramatsu, M, Okuno, M, et al. (2011) GLP-1 secretion in response to oral and luminal palatinose (isomaltulose) in rats. J Nutr Sci Vitaminol (Tokyo) 57, 3035.
33 Chen, W, Hira, T, Nakajima, S, et al. (2012) Suppressive effect on food intake of a potato extract (Potein®) involving cholecystokinin release in rats. Biosci Biotechnol Biochem 76, 11041109.
34 Kokrashvili, Z, Mosinger, B & Margolskee, RF (2009) T1r3 and α-gustducin in gut regulate secretion of glucagon-like peptide-1. Ann N Y Acad Sci 1170, 9194.
35 Shirazi-Beechey, SP, Daly, K, Al-Rammahi, M, et al. (2014) Role of nutrient-sensing taste 1 receptor (T1R) family members in gastrointestinal chemosensing. Br J Nutr 111, Suppl. 1, S8S15.
36 Vogt, LM, Meyer, D, Pullens, G, et al. (2014) Toll-like receptor 2 activation by β2 → 1-fructans protects barrier function of T84 human intestinal epithelial cells in a chain length-dependent manner. J Nutr 144, 10021008.
37 Rocca, AS & Brubaker, PL (1999) Role of the vagus nerve in mediating proximal nutrient-induced glucagon-like peptide-1 secretion. Endocrinology 140, 16871694.
38 Sarwar, G (1997) The protein digestibility-corrected amino acid score method overestimates quality of proteins containing antinutritional factors and of poorly digestible proteins supplemented with limiting amino acids in rats. J Nutr 127, 758764.
39 Everard, A & Cani, PD (2014) Gut microbiota and GLP-1. Rev Endocr Metab Disord 15, 189196.
40 Nøhr, MK, Pedersen, MH, Gille, A, et al. (2013) GPR41/FFAR3 and GPR43/FFAR2 as cosensors for short-chain fatty acids in enteroendocrine cells vs FFAR3 in enteric neurons and FFAR2 in enteric leukocytes. Endocrinology 154, 35523564.
41 Matsukawa, N, Matsumoto, M, Shinoki, A, et al. (2009) Nondigestible saccharides suppress the bacterial degradation of quercetin aglycone in the large intestine and enhance the bioavailability of quercetin glucoside in rats. J Agric Food Chem 57, 94629468.
42 Campbell, JM, Fahey, GC & Wolf, BW (1997) Selected indigestible oligosaccharides affect large bowel mass, cecal and fecal short-chain fatty acids, pH and microflora in rats. J Nutr 127, 130136.
43 Mansour, A, Hosseini, S, Larijani, B, et al. (2013) Nutrients related to GLP1 secretory responses. Nutrition 29, 813820.
44 Kishimoto, Y, Kanahori, S, Sakano, K, et al. (2013) The maximum single dose of resistant maltodextrin that does not cause diarrhea in humans. J Nutr Sci Vitaminol (Tokyo) 59, 352357.
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