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Resistant maltodextrin or fructooligosaccharides promotes GLP-1 production in male rats fed a high-fat and high-sucrose diet, and partially reduces energy intake and adiposity

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Abstract

Purpose

Increasing secretion and production of glucagon-like peptide-1 (GLP-1) by continuous ingestion of certain food components has been expected to prevent glucose intolerance and obesity. In this study, we examined whether a physiological dose (5% weight in diet) of digestion-resistant maltodextrin (RMD) has a GLP-1-promoting effect in rats fed a high-fat and high-sucrose (HFS) diet.

Methods

Rats were fed a control diet or the HFS (30% fat, 40% sucrose wt/wt) diet supplemented with 5% RMD or fructooligosaccharides (FOS) for 8 weeks or for 8 days in separated experiments. Glucose tolerance, energy intake, plasma and tissue GLP-1 concentrations, and cecal short-chain fatty acids concentrations were assessed.

Results

After 4 weeks of feeding, HFS-fed rats had significantly higher glycemic response to oral glucose than control rats, but rats fed HFS + RMD/FOS did not (approx. 50% reduction vs HFS rats). HFS + RMD/FOS-fed rats had higher GLP-1 responses (~twofold) to oral glucose, than control rats. After 8 weeks, visceral adipose tissue weight was significantly higher in HFS-fed rats than control rats, while HFS + RMD/FOS rats had a trend of reduced gain (~50%) of the tissue weight. GLP-1 contents and luminal propionate concentrations in the large intestine increased (>twofold) by adding RMD/FOS to HFS. Eight days feeding of RMD/FOS-supplemented diets reduced energy intake (~10%) and enhanced cecal GLP-1 production (~twofold), compared to HFS diet.

Conclusions

The physiological dose of a prebiotic fiber promptly (within 8 days) promotes GLP-1 production in rats fed an obesogenic diet, which would help to prevent excess energy intake and fat accumulation.

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Abbreviations

HFS:

High-fat and high-sucrose

GLP-1:

Glucagon-like peptide-1

RMD:

Resistant maltodextrin

FOS:

Fructooligosaccharides

GIP:

Glucose-dependent insulinotropic polypeptide

OGTT:

Oral glucose tolerance test

PYY:

Peptide YY

DPP-IV:

Dipeptidyl peptidase-IV

SCFA:

Short-chain fatty acid

References

  1. Cho YM, Fujita Y, Kieffer TJ (2014) Glucagon-like peptide-1: glucose homeostasis and beyond. Annu Rev Physiol 76:535–559. doi:10.1146/annurev-physiol-021113-170315

    Article  CAS  Google Scholar 

  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(8):G759–G761. doi:10.1152/ajpgi.00078.2012

    Article  CAS  Google Scholar 

  3. Nauck M (2016) Incretin therapies: highlighting common features and differences in the modes of action of glucagon-like peptide-1 receptor agonists and dipeptidyl peptidase-4 inhibitors. Diabetes Obes Metab 18(3):203–216. doi:10.1111/dom.12591

    Article  CAS  Google Scholar 

  4. Diakogiannaki E, Gribble FM, Reimann F (2012) Nutrient detection by incretin hormone secreting cells. Physiol Behav 106(3):387–393. doi:10.1016/j.physbeh.2011.12.001

    Article  CAS  Google Scholar 

  5. Higuchi N, Hira T, Yamada N, Hara H (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(9):3089–3098. doi:10.1210/en.2012-2275

    Article  CAS  Google Scholar 

  6. Ishikawa Y, Hira T, Inoue D, Harada Y, Hashimoto H, Fujii M, Kadowaki M, Hara H (2015) Rice protein hydrolysates stimulate GLP-1 secretion, reduce GLP-1 degradation, and lower the glycemic response in rats. Food Funct 6(8):2525–2534. doi:10.1039/c4fo01054j

    Article  CAS  Google Scholar 

  7. Greenfield JR, Farooqi IS, Keogh JM, Henning E, Habib AM, Blackwood A, Reimann F, Holst JJ, Gribble FM (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(1):106–113. doi:10.3945/ajcn.2008.26362

    Article  CAS  Google Scholar 

  8. Jakubowicz D, Froy O, Ahrén B, Boaz M, Landau Z, Bar-Dayan Y, Ganz T, Barnea M, Wainstein J (2014) Incretin, insulinotropic and glucose-lowering effects of whey protein pre-load in type 2 diabetes: a randomised clinical trial. Diabetologia 57(9):1807–1811. doi:10.1007/s00125-014-3305-x

    Article  CAS  Google Scholar 

  9. Hira T, Ikee A, Kishimoto Y, Kanahori S, Hara H (2015) Resistant maltodextrin promotes fasting glucagon-like peptide-1 secretion and production together with glucose tolerance in rats. Br J Nutr 114(1):34–42. doi:10.1017/S0007114514004322

    Article  CAS  Google Scholar 

  10. 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(3):521–526

    Article  CAS  Google Scholar 

  11. Cani PD, Daubioul CA, Reusens B, Remacle C, Catillon G, Delzenne NM (2005) Involvement of endogenous glucagon-like peptide-1(7–36) amide on glycaemia-lowering effect of oligofructose in streptozotocin-treated rats. J Endocrinol 185(3):457–465. doi:10.1677/joe.1.06100

    Article  CAS  Google Scholar 

  12. Delzenne NM, Cani PD, Daubioul C, Neyrinck AM (2005) Impact of inulin and oligofructose on gastrointestinal peptides. Br J Nutr 93(Suppl 1):S157–S161

    Article  CAS  Google Scholar 

  13. Fastinger ND, Karr-Lilienthal LK, Spears JK, Swanson KS, Zinn KE, Nava GM, Ohkuma K, Kanahori S, Gordon DT, Fahey GC (2008) A novel resistant maltodextrin alters gastrointestinal tolerance factors, fecal characteristics, and fecal microbiota in healthy adult humans. J Am Coll Nutr 27(2):356–366

    Article  CAS  Google Scholar 

  14. 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(1):40–46. doi:10.1038/oby.2007.16

    Article  CAS  Google Scholar 

  15. Zhou J, Martin RJ, Tulley RT, Raggio AM, McCutcheon KL, Shen L, Danna SC, Tripathy S, Hegsted M, Keenan MJ (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(5):E1160–E1166. doi:10.1152/ajpendo.90637.2008

    Article  CAS  Google Scholar 

  16. Hashizume C, Kishimoto Y, Kanahori S, Yamamoto T, Okuma K, Yamamoto K (2012) Improvement effect of resistant maltodextrin in humans with metabolic syndrome by continuous administration. J Nutr Sci Vitaminol (Tokyo) 58(6):423–430

    Article  CAS  Google Scholar 

  17. 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(1):114–125. doi:10.3945/ajcn.2008.26842

    Article  CAS  Google Scholar 

  18. Chu HF, Pan MH, Ho CT, Tseng YH, Wang WW, Chau CF (2014) Variations in the efficacy of resistant maltodextrin on body fat reduction in rats fed different high-fat models. J Agric Food Chem 62(1):192–197. doi:10.1021/jf404809v

    Article  CAS  Google Scholar 

  19. Ye Z, Arumugam V, Haugabrooks E, Williamson P, Hendrich S (2015) Soluble dietary fiber (Fibersol-2) decreased hunger and increased satiety hormones in humans when ingested with a meal. Nutr Res 35(5):393–400. doi:10.1016/j.nutres.2015.03.004

    Article  Google Scholar 

  20. Adam CL, Gratz SW, Peinado DI, Thomson LM, Garden KE, Williams PA, Richardson AJ, Ross AW (2016) Effects of dietary fibre (Pectin) and/or increased protein (Casein or Pea) on satiety, body weight, adiposity and caecal fermentation in high fat diet-induced obese rats. PLoS One 11(5):e0155871. doi:10.1371/journal.pone.0155871

    Article  Google Scholar 

  21. den Besten G, Gerding A, van Dijk TH, Ciapaite J, Bleeker A, van Eunen K, Havinga R, Groen AK, Reijngoud DJ, Bakker BM (2015) Protection against the metabolic syndrome by guar gum-derived short-chain fatty acids depends on peroxisome proliferator-activated receptor γ and glucagon-like peptide-1. PLoS One 10(8):e0136364. doi:10.1371/journal.pone.0136364

    Article  Google Scholar 

  22. Adam CL, Williams PA, Dalby MJ, Garden K, Thomson LM, Richardson AJ, Gratz SW, Ross AW (2014) Different types of soluble fermentable dietary fibre decrease food intake, body weight gain and adiposity in young adult male rats. Nutr Metab (Lond) 11:36. doi:10.1186/1743-7075-11-36

    Article  Google Scholar 

  23. Parnell JA, Reimer RA (2012) Prebiotic fiber modulation of the gut microbiota improves risk factors for obesity and the metabolic syndrome. Gut Microbes 3(1):29–34. doi:10.4161/gmic.19246

    Article  Google Scholar 

  24. Cluny NL, Eller LK, Keenan CM, Reimer RA, Sharkey KA (2015) Interactive effects of oligofructose and obesity predisposition on gut hormones and microbiota in diet-induced obese rats. Obesity (Silver Spring) 23(4):769–778. doi:10.1002/oby.21017

    Article  CAS  Google Scholar 

  25. Turner ND, Lupton JR (2011) Dietary fiber. Adv Nutr 2(2):151–152. doi:10.3945/an.110.000281

    Article  Google Scholar 

  26. Reeves PG (1997) Components of the AIN-93 diets as improvements in the AIN-76A diet. J Nutr 127(5 Suppl):838 S–841 S

    Article  CAS  Google Scholar 

  27. Cani PD, Hoste S, Guiot Y, Delzenne NM (2007) Dietary non-digestible carbohydrates promote L-cell differentiation in the proximal colon of rats. Br J Nutr 98(1):32–37. doi:10.1017/S0007114507691648

    Article  CAS  Google Scholar 

  28. Iwaya H, Lee JS, Yamagishi S, Shinoki A, Lang W, Thawornkuno C, Kang HK, Kumagai Y, Suzuki S, Kitamura S, Hara H, Okuyama M, Mori H, Kimura A, Ishizuka S (2012) The delay in the development of experimental colitis from isomaltosyloligosaccharides in rats is dependent on the degree of polymerization. PLoS One 7(11):e50658. doi:10.1371/journal.pone.0050658

    Article  CAS  Google Scholar 

  29. Miyazato S, Nakagawa C, Kishimoto Y, Tagami H, Hara H (2010) Promotive effects of resistant maltodextrin on apparent absorption of calcium, magnesium, iron and zinc in rats. Eur J Nutr 49(3):165–171. doi:10.1007/s00394-009-0062-6

    Article  CAS  Google Scholar 

  30. Cacho J, Sevillano J, de Castro J, Herrera E, M. P. Ramos (2108) Validation of simple indexes to assess insulin sensitivity during pregnancy in Wistar and Sprague-Dawley rats. Am J Physiol Endocrinol Metab 295:E1269–E1276. doi:10.1152/ajpendo.90207.2008

  31. Tappy L, Lê KA (2010) Metabolic effects of fructose and the worldwide increase in obesity. Physiol Rev 90(1):23–46. doi:10.1152/physrev.00019.2009

    Article  CAS  Google Scholar 

  32. Micha R, Khatibzadeh S, Shi P, Fahimi S, Lim S, Andrews KG, Engell RE, Powles J, Ezzati M, Mozaffarian D, NutriCoDE GBoDNaCDEG (2014) Global, regional, and national consumption levels of dietary fats and oils in 1990 and 2010: a systematic analysis including 266 country-specific nutrition surveys. BMJ 348:g2272. doi:10.1136/bmj.g2272

    Article  Google Scholar 

  33. Lai M, Chandrasekera PC, Barnard ND (2014) You are what you eat, or are you? The challenges of translating high-fat-fed rodents to human obesity and diabetes. Nutr Diabetes 4:e135. doi:10.1038/nutd.2014.30

    Article  CAS  Google Scholar 

  34. Nakajima S, Hira T, Hara H (2015) Postprandial glucagon-like peptide-1 secretion is increased during the progression of glucose intolerance and obesity in high-fat/high-sucrose diet-fed rats. Br J Nutr 113(9):1477–1488. doi:10.1017/S0007114515000550

    Article  CAS  Google Scholar 

  35. Theodorakis MJ (2015) Comment on Færch et al. GLP-1 Response to Oral Glucose Is Reduced in Prediabetes, Screen-Detected Type 2 Diabetes, and Obesity and Influenced by Sex: The ADDITION-PRO Study. Diabetes 2015;64:2513–2525. Diabetes 64(9):e28–29. doi:10.2337/db15-0614. (discussion e30–21)

    Article  CAS  Google Scholar 

  36. Færch K, Torekov SS, Vistisen D, Johansen NB, Witte DR, Jonsson A, Pedersen O, Hansen T, Lauritzen T, Sandbæk A, Holst JJ, Jørgensen ME (2015) GLP-1 response to oral glucose is reduced in prediabetes, screen-detected type 2 diabetes, and obesity and influenced by sex: The ADDITION-PRO Study. Diabetes 64(7):2513–2525. doi:10.2337/db14-1751

    Article  Google Scholar 

  37. Smushkin G, Sathananthan A, Man CD, Zinsmeister AR, Camilleri M, Cobelli C, Rizza RA, Vella A (2012) Defects in GLP-1 response to an oral challenge do not play a significant role in the pathogenesis of prediabetes. J Clin Endocrinol Metab 97(2):589–598. doi:10.1210/jc.2011-2561

    Article  CAS  Google Scholar 

  38. Numao S, Kawano H, Endo N, Yamada Y, Konishi M, Takahashi M, Sakamoto S (2012) Short-term low carbohydrate/high-fat diet intake increases postprandial plasma glucose and glucagon-like peptide-1 levels during an oral glucose tolerance test in healthy men. Eur J Clin Nutr 66(8):926–931. doi:10.1038/ejcn.2012.58

    Article  CAS  Google Scholar 

  39. Trevaskis JL, Griffin PS, Wittmer C, Neuschwander-Tetri BA, Brunt EM, Dolman CS, Erickson MR, Napora J, Parkes DG, Roth JD (2012) Glucagon-like peptide-1 receptor agonism improves metabolic, biochemical, and histopathological indices of nonalcoholic steatohepatitis in mice. Am J Physiol Gastrointest Liver Physiol 302(8):G762–G772. doi:10.1152/ajpgi.00476.2011

    Article  CAS  Google Scholar 

  40. Wu H, Sui C, Xu H, Xia F, Zhai H, Zhang H, Weng P, Han B, Du S, Lu Y (2014) The GLP-1 analogue exenatide improves hepatic and muscle insulin sensitivity in diabetic rats: tracer studies in the basal state and during hyperinsulinemic-euglycemic clamp. J Diabetes Res 2014:524517. doi:10.1155/2014/524517

    Google Scholar 

  41. Kishimoto Y, Oga H, Tagami H, Okuma K, Gordon DT (2007) Suppressive effect of resistant maltodextrin on postprandial blood triacylglycerol elevation. Eur J Nutr 46(3):133–138. doi:10.1007/s00394-007-0643-1

    Article  CAS  Google Scholar 

  42. Beylot M (2005) Effects of inulin-type fructans on lipid metabolism in man and in animal models. Br J Nutr 93(Suppl 1):S163–S168

    Article  CAS  Google Scholar 

  43. Phuwamongkolwiwat P, Suzuki T, Hira T, Hara H (2014) Fructooligosaccharide augments benefits of quercetin-3-O-β-glucoside on insulin sensitivity and plasma total cholesterol with promotion of flavonoid absorption in sucrose-fed rats. Eur J Nutr 53(2):457–468. doi:10.1007/s00394-013-0546-2

    Article  CAS  Google Scholar 

  44. Cani PD, Knauf C, Iglesias MA, Drucker DJ, Delzenne NM, Burcelin R (2006) Improvement of glucose tolerance and hepatic insulin sensitivity by oligofructose requires a functional glucagon-like peptide 1 receptor. Diabetes 55(5):1484–1490

    Article  CAS  Google Scholar 

  45. Cani PD, Neyrinck AM, Maton N, Delzenne NM (2005) Oligofructose promotes satiety in rats fed a high-fat diet: involvement of glucagon-like Peptide-1. Obes Res 13(6):1000–1007. doi:10.1038/oby.2005.117

    Article  CAS  Google Scholar 

  46. Verhoef SP, Meyer D, Westerterp KR (2011) Effects of oligofructose on appetite profile, glucagon-like peptide 1 and peptide YY3-36 concentrations and energy intake. Br J Nutr 106(11):1757–1762. doi:10.1017/S0007114511002194

    Article  CAS  Google Scholar 

  47. Liber A, Szajewska H (2013) Effects of inulin-type fructans on appetite, energy intake, and body weight in children and adults: systematic review of randomized controlled trials. Ann Nutr Metab 63(1–2):42–54. doi:10.1159/000350312

    Article  CAS  Google Scholar 

  48. Pedersen C, Lefevre S, Peters V, Patterson M, Ghatei MA, Morgan LM, Frost GS (2013) Gut hormone release and appetite regulation in healthy non-obese participants following oligofructose intake. A dose-escalation study. Appetite 66:44–53. doi:10.1016/j.appet.2013.02.017

    Article  Google Scholar 

  49. Daud NM, Ismail NA, Thomas EL, Fitzpatrick JA, Bell JD, Swann JR, Costabile A, Childs CE, Pedersen C, Goldstone AP, Frost GS (2014) The impact of oligofructose on stimulation of gut hormones, appetite regulation and adiposity. Obesity (Silver Spring) 22(6):1430–1438. doi:10.1002/oby.20754

    Article  CAS  Google Scholar 

  50. Tolhurst G, Heffron H, Lam YS, Parker HE, Habib AM, Diakogiannaki E, Cameron J, Grosse J, Reimann F, Gribble FM (2012) Short-chain fatty acids stimulate glucagon-like peptide-1 secretion via the G-protein-coupled receptor FFAR2. Diabetes 61(2):364–371. doi:10.2337/db11-1019

    Article  CAS  Google Scholar 

  51. Psichas A, Sleeth ML, Murphy KG, Brooks L, Bewick GA, Hanyaloglu AC, Ghatei MA, Bloom SR, Frost G (2015) The short chain fatty acid propionate stimulates GLP-1 and PYY secretion via free fatty acid receptor 2 in rodents. Int J Obes (Lond) 39(3):424–429. doi:10.1038/ijo.2014.153

    Article  CAS  Google Scholar 

  52. Chambers ES, Viardot A, Psichas A, Morrison DJ, Murphy KG, Zac-Varghese SE, MacDougall K, Preston T, Tedford C, Finlayson GS, Blundell JE, Bell JD, Thomas EL, Mt-Isa S, Ashby D, Gibson GR, Kolida S, Dhillo WS, Bloom SR, Morley W, Clegg S, Frost G (2015) Effects of targeted delivery of propionate to the human colon on appetite regulation, body weight maintenance and adiposity in overweight adults. Gut 64(11):1744–1754. doi:10.1136/gutjnl-2014-307913

    Article  CAS  Google Scholar 

  53. Byrne CS, Chambers ES, Morrison DJ, Frost G (2015) The role of short chain fatty acids in appetite regulation and energy homeostasis. Int J Obes (Lond) 39(9):1331–1338. doi:10.1038/ijo.2015.84

    Article  CAS  Google Scholar 

  54. Svendsen B, Pedersen J, Albrechtsen NJ, Hartmann B, Toräng S, Rehfeld JF, Poulsen SS, Holst JJ (2015) An analysis of cosecretion and coexpression of gut hormones from male rat proximal and distal small intestine. Endocrinology 156(3):847–857. doi:10.1210/en.2014-1710

    Article  CAS  Google Scholar 

  55. Rouillé Y, Kantengwa S, Irminger JC, Halban PA (1997) Role of the prohormone convertase PC3 in the processing of proglucagon to glucagon-like peptide 1. J Biol Chem 272(52):32810–32816

    Article  Google Scholar 

  56. Morimoto K, Watanabe M, Sugizaki T, Irie J, Itoh H (2016) Intestinal bile acid composition modulates prohormone convertase 1/3 (PC1/3) expression and consequent GLP-1 production in male mice. Endocrinology 157(3):1071–1081. doi:10.1210/en.2015-1551

    Article  CAS  Google Scholar 

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Correspondence to Tohru Hira.

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The research was supported by JSPS KAKENHI Grant No. 26252016.

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Y. Kishimoto and S. Kanahori are employees of Matsutani Chemical Industry. T. Hira, R. Suto, and H. Hara, no conflicts of interest.

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Hira, T., Suto, R., Kishimoto, Y. et al. Resistant maltodextrin or fructooligosaccharides promotes GLP-1 production in male rats fed a high-fat and high-sucrose diet, and partially reduces energy intake and adiposity. Eur J Nutr 57, 965–979 (2018). https://doi.org/10.1007/s00394-017-1381-7

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