Anti-diabetic effects of the soluble dietary fiber from tartary buckwheat bran in diabetic mice and their potential mechanisms

  • Weijing Wu Department of Public Health and Medical Technology, Xiamen Medical College, Xiamen, Fujian, and Fujian Provincial Key Laboratory of Food Microbiology and Enzyme Engineering, Xiamen, Fujian, China
  • Zaigui Li College of Food Science and Nutritional Engineering, China Agricultural University, Haidian, Beijing, China
  • Fei Qin Department of Public Health and Medical Technology, Xiamen Medical College, Xiamen, Fujian, China
  • Ju Qiu Institute of Food and Nutrition Development, Ministry of Agriculture and Rural Affairs, Haidian, Beijing, China
DOI: https://doi.org/10.29219/fnr.v65.4998
Keywords: Soluble dietary fiber, tartary buckwheat, glucose metabolism, lipid metabolism, short-chain fatty acids, AMP-activated protein kinase

Abstract

Background: Tartary buckwheat has beneficial effects on glucose and lipid metabolism of patients with type 2 diabetes mellitus. However, the physiological effects of a soluble dietary fiber (SDF) from tartary buckwheat have rarely been studied, especially in vivo.

Objective: This study aimed to examine the hypoglycemic and hypolipidemic effects of SDF from tartary buckwheat bran on high-fat diet/streptozotocin-induced diabetic mice.

Design: The SDF of tartary buckwheat bran was collected according to the Association of Official Analytical Chemists method 991.43. Diabetic mice were treated with high-fat diets supplemented with 0.5, 1, and 2% SDF for 8 weeks. Parameters related to glucose and lipid metabolism and relevant mechanisms, including the excretion of short-chain fatty acids and the glycemic signaling pathway in the liver, were investigated. In addition, the structural characterization of a purified polysaccharide from SDF of tartary buckwheat bran was illustrated.

Result: Supplementation with SDF in the diet resulted in reduced levels of fasting blood glucose, improved oral glucose tolerance, increased levels of liver glycogen and insulin, as well as improved lipid profiles in both the serum and liver, in diabetic mice. The amelioration of glucose and lipid metabolism by SDF was accompanied by an increase in the short-chain fatty acid levels in the cecum and co-regulated by hepatic adenosine- 5′-monophosphate-activated protein kinase (AMPK) phosphorylation. A neutral tartary buckwheat polysaccharide with an average molecular weight of 19.6 kDa was purified from the SDF, which consisted mainly of glucose with α-glycosidic bonds.

Conclusions: The SDF of tartary buckwheat bran exhibits hypoglycemic and hypolipidemic effects in diabetic mice, contributing to the anti-diabetic mechanisms of tartary buckwheat.

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References


  1. Kahn SE, Cooper ME, Del Prato S. Pathophysiology and treatment of type 2 diabetes: perspectives on the past, present, and future. Lancet 2014; 383(9922): 1068–83. doi: 10.1016/S0140-6736(13)62154-6

  2. Yao B, Fang H, Xu W, Yan Y, Xu H, Liu Y, et al. Dietary fiber intake and risk of type 2 diabetes: a dose-response analysis of prospective studies. Eur J Epidemiol 2014; 29(2): 79–88. doi: 10.1007/s10654-013-9876-x

  3. Alvarez-Jubete L, Arendt E, Gallagher E. Nutritive value and chemical composition of pseudocereals as gluten-free ingredients. Int J Food Sci Nutr 2009; 60(sup4): 240–57. doi: 10.1080/09637480902950597

  4. Zhu F. Dietary fiber polysaccharides of amaranth, buckwheat and quinoa grains: a review of chemical structure, biological functions and food uses. Carbohyd Polym 2020; 248: 116819. doi: 10.1016/j.carbpol.2020.116819

  5. Ciudad-Mulero M, Fernández-Ruiz V, Matallana-González MC, Morales P. Dietary fiber sources and human benefits: the case study of cereal and pseudocereals. Adv Food Nutr Res 2019; 90: 83–134. doi: 10.1016/bs.afnr.2019.02.002

  6. Qiu J, Liu Y, Yue Y, Qin Y, Li Z. Dietary tartary buckwheat intake attenuates insulin resistance and improves lipid profiles in patients with type 2 diabetes: a randomized controlled trial. Nutr Res 2016; 36(12): 1392–401. doi: 10.1016/j.nutres.2016.11.007

  7. Bonafaccia G, Marocchini M, Kreft I. Composition and technological properties of the flour and bran from common and tartary buckwheat. Food Chem 2003; 80(1): 9–15. doi: 10.1016/S0308-8146(02)00228-5

  8. Wang XT, Zhu ZY, Zhao L, Sun HQ, Meng M, Zhang JY, et al. Structural characterization and inhibition on α-d-glucosidase activity of non-starch polysaccharides from Fagopyrum tartaricum. Carbohydr Polym 2016; 153: 679–85. doi: 10.1016/j.carbpol.2016.08.024

  9. Tong L-T, Wang L, Zhou X, Zhong K, Liu L, Wang F, et al. Antitumor activity of Dendrobium devonianum polysaccharides based on its immunomodulatory effects in S180 tumor-bearing mice. RSC Advances 2016; 6(46): 40250–7. doi: 10.1039/C6RA03074B

  10. Shen RL, Cai FL, Dong JL, Hu XZ. Hypoglycemic effects and biochemical mechanisms of oat products on streptozotocin-induced diabetic mice. J Agric Food Chem 2011; 59(16): 8895–900. doi: 10.1021/jf200678q

  11. Wei CY, Liao NB, Zhang Y, Ye XQ, Li S, Hu YQ, et al. In vitro fermentation behaviors of fucosylated chondroitin sulfate from Pearsonothuria graeffei by human gut microflora. Int J Biol Macromol 2017; 102: 1195–201. doi: 10.1016/j.ijbiomac.2017.04.036

  12. Carvalho BM, Guadagnini D, Tsukumo DML, Schenka AA, Latuf-Filho P, Vassallo J, et al. Modulation of gut microbiota by antibiotics improves insulin signalling in high-fat fed mice. Diabetologia 2012; 55(10): 2823–34. doi: 10.1007/s00125-012-2648-4

  13. Jiao D, Meng Y, Liu L, Li J, Ren D, Guo Y. Purification, characterization and antioxidant activities of polysaccharides from thinned-young apple. Int J Biol Macromol 2015; 72: 31–40. doi: 10.1016/j.ijbiomac.2014.07.053

  14. Zou S, Zhang X, Yao W, Niu Y, Gao X. Structure characterization and hypoglycemic activity of a polysaccharide isolated from the fruit of Lycium barbarum L. Carbohydr Polym 2010; 80(4): 1161–7. doi: 10.1016/j.carbpol.2010.01.038

  15. Ren YY, Zhu ZY, Sun HQ, Chen LJ. Structural characterization and inhibition on α-glucosidase activity of acidic polysaccharide from Annona squamosa. Carbohydr Polym 2017; 174: 1. doi: 10.1016/j.carbpol.2017.05.092

  16. Luo AX, He XJ, Zhou SD, Fan YJ, Luo AS, Chun Z. Purification, composition analysis and antioxidant activity of the polysaccharides from Dendrobium nobile Lindl. Carbohydr Polym 2010; 79(4): 1014–9. doi: 10.1016/j.carbpol.2009.10.033

  17. Dong Q, Yao J, Yang XT, Fang JN. Structural characterization of a water-soluble β- d -glucan from fruiting bodies of Agaricus blazei Murr. Carbohydr Res 2002; 337(15): 1417–21. doi: 10.1016/S0008-6215(02)00166-0

  18. Chen X, Cao D, Zhou L, Jin H, Dong Q, Yao J, et al. Structure of a polysaccharide from Gastrodia elata Bl., and oligosaccharides prepared thereof with anti-pancreatic cancer cell growth activities. Carbohydr Polym 2011; 86(3): 1300–5. doi: 10.1016/j.carbpol.2011.06.029

  19. Pfeiffer P, Valentine K, Parrish F. Additions and corrections – deuterium-induced differential isotope shift 13 C NMR. I. Resonance reassignments of mono and disaccharides. J Am Chem Soc 1979; 101(24): 7438. doi: 10.1021/ja00518a604

  20. Usui T, Yamaoka N, Matsuda K, Tuzimura K, Sugiyama H, Seto S. 13 C nuclear magnetic resonance spectra of glucobioses, glucotrioses, and glucans. J Chem Soc, Perkin Trans 1973; 1: 2425–32. doi: 10.1002/chin.197402069

  21. Heyraud A, Rinaudo M, Vignon M, Vincendon M. 13C-NMR spectroscopic investigation of α- and β-1,4-D-glucose homooligomers. Biopolymers 1979; 18(1): 167–85. doi: 10.1002/bip.1979.360180113

  22. Dong J, Cai F, Shen R, Liu Y. Hypoglycaemic effects and inhibitory effect on intestinal disaccharidases of oat beta-glucan in streptozotocin-induced diabetic mice. Food Chem 2011; 129(3): 1066–71. doi: 10.1016/j.foodchem.2011.05.076

  23. Liu M, Zhang Y, Zhang H, Hu B, Wang L, Qian H, et al. The anti-diabetic activity of oat β-d-glucan in streptozotocin–nicotinamide induced diabetic mice. Int J Biol Macromol 2016; 91: 1170–6. doi: 10.1016/j.ijbiomac.2016.06.083

  24. Ma M, Mu T. Anti-diabetic effects of soluble and insoluble dietary fibre from deoiled cumin in low-dose streptozotocin and high glucose-fat diet-induced type 2 diabetic rats. J Funct Foods 2016; 25: 186–96. doi: 10.1016/j.jff.2016.05.011

  25. Li L, Pan M, Pan S, Li W, Zhong Y, Hu J, et al. Effects of insoluble and soluble fibers isolated from barley on blood glucose, serum lipids, liver function and caecal short-chain fatty acids in type 2 diabetic and normal rats. Food Chem Toxicol 2020; 135: 110937. doi: 10.1016/j.fct.2019.110937

  26. Zheng Y, Wang Q, Huang J, Fang D, Zhuang W, Luo X, et al. Hypoglycemic effect of dietary fibers from bamboo shoot shell: an in vitro and in vivo study. Food Chem Toxicol 2019; 127: 120–6. doi: 10.1016/j.fct.2019.03.008

  27. Ou S, Kwok K-c, Li Y, Fu L. In vitro study of possible role of dietary fiber in lowering postprandial serum glucose. J Agric Food Chem 2001; 49(2): 1026–9. doi: 10.1021/jf000574n

  28. Li Q, Wu T, Liu R, Zhang M, Wang R. Soluble dietary fiber reduces trimethylamine metabolism via gut microbiota and co-regulates host AMPK pathways. Mol Nutr Food Res 2017; 61(12): 1700473. doi: 10.1002/mnfr.201700473

  29. Gao Z, Yin J, Zhang J, Ward RE, Martin RJ, Lefevre M, et al. Butyrate improves insulin sensitivity and increases energy expenditure in mice. Diabetes 2009; 58(7): 1509–17. doi: 10.2337/db08-1637

  30. Li L, He M, Xiao H, Liu X, Wang K, Zhang Y. Acetic acid influences BRL-3A cell lipid metabolism via the AMPK signalling pathway. Cell Physiol Biochem 2018; 45(5): 2021–30. doi: 10.1159/000487980

  31. Hu G-X, Chen G-R, Xu H, Ge R-S, Lin J. Activation of the AMP activated protein kinase by short-chain fatty acids is the main mechanism underlying the beneficial effect of a high fiber diet on the metabolic syndrome. Med Hypotheses 2010; 74(1): 123–6. doi: 10.1016/j.mehy.2009.07.022

  32. den Besten G, Gerding A, van Dijk TH, Ciapaite J, Bleeker A, van Eunen K, et al. 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 2015; 10(8): e0136364. doi: 10.1371/journal.pone.0136364

  33. Rosado CP, Rosa VHC, Martins BC, Soares AC, Santos IB, Monteiro EB, et al. Resistant starch from green banana (Musa sp.) attenuates non-alcoholic fat liver accumulation and increases short-chain fatty acids production in high-fat diet-induced obesity in mice. Int J Biol Macromol 2020; 145: 1066–72. doi: 10.1016/j.ijbiomac.2019.09.199

  34. Shtriker MG, Hahn M, Taieb E, Nyska A, Moallem U, Tirosh O, et al. Fenugreek galactomannan and citrus pectin improve several parameters associated with glucose metabolism and modulate gut microbiota in mice. Nutrition 2018; 46: 134–42. doi: 10.1016/j.nut.2017.07.012

  35. Hardie DG. AMP-activated protein kinase: a master switch in glucose and lipid metabolism. Rev Endocr Metab Disord 2004; 5(2): 119–25. doi: 10.1023/B:REMD.0000021433.63915.bb

  36. Sakakibara S, Yamauchi T, Oshima Y, Tsukamoto Y, Kadowaki T. Acetic acid activates hepatic AMPK and reduces hyperglycemia in diabetic KK-A(y) mice. Biochem Biophys Res Commun 2006; 344(2): 597–604. doi: 10.1016/j.bbrc.2006.03.176

  37. Tomoo K, Mikiya K, Takashi F, Takayuki K. Acetic acid upregulates the expression of genes for fatty acid oxidation enzymes in liver to suppress body fat accumulation. J Agric Food Chem 2009; 57(13): 5982. doi: 10.1021/jf900470c

  38. Benoit V, Marc F, Bruno G, Sandrine H, Renaud D, Luc B, et al. Activation of AMP-activated protein kinase in the liver: a new strategy for the management of metabolic hepatic disorders. J Physiol Sci 2010; 574(1): 41–53. doi:

  39. Morrison DJ, Preston T. Formation of short chain fatty acids by the gut microbiota and their impact on human metabolism. Gut Microbes 2016; 7(3): 189–200. doi: 10.1080/19490976.2015.1134082

  40. White AM, Johnston CS. Vinegar ingestion at bedtime moderates waking glucose concentrations in adults with well-controlled type 2 diabetes. Diabetes Care 2007; 30(11): 2814–5. doi: 10.2337/dc07-1062

  41. Yoshida H, Ishii M, Akagawa M. Propionate suppresses hepatic gluconeogenesis via GPR43/AMPK signaling pathway. Arch Biochem Biophys 2019; 672: 108057. doi: 10.1016/j.abb.2019.07.022

  42. Nanao H, Hideyuki S, Akifumi K, Hiraku O, Midori F, Hideaki K, et al. AMP-activated protein kinase activation increases phosphorylation of glycogen synthase kinase 3beta and thereby reduces cAMP-responsive element transcriptional activity and phosphoenolpyruvate carboxykinase C gene expression in the liver. J Biol Chem 2008; 283(49): 33902–10. doi: 10.1074/jbc.M802537200

  43. Chen Y, Ye R, Luo Y, Zhang N. Novel blasting extrusion processing improved the physicochemical properties of soluble dietary fiber from soybean residue and in vivo evaluation. J Food Eng 2014; 120(1): 1–8. doi: 10.1016/j.jfoodeng.2013.07.011

  44. Saeed S, Mosa-Al-Reza H, Fatemeh AN, Saeideh D. Antihyperglycemic and antihyperlipidemic effects of guar gum on streptozotocin-induced diabetes in male rats. Pharmacogn Mag 2012; 8(29): 65. doi: 10.4103/0973-1296.93328

  45. Hara H, Haga S, Aoyama Y, Kiriyama S. Short-chain fatty acids suppress cholesterol synthesis in rat liver and intestine. J Nutr 1999; 129(5): 942–8. doi: 10.1038/sj.ijo.0800911

  46. Gijs DB, Aycha B, Albert G, Karen VE, Rick H, Dijk TH, Van, et al. Short-chain fatty acids protect against high-fat diet-induced obesity via a PPARγ-dependent switch from lipogenesis to fat oxidation. Diabetes 2015; 64(7): 2398–408. doi: 10.2337/db14-1213

  47. Wang X, Shi L, Wang X, Feng Y, Wang Y. MDG-1, an Ophiopogon polysaccharide, restrains process of non-alcoholic fatty liver disease via modulating the gut-liver axis. Int J Biol Macromol 2019; 141: 1013–21. doi: 10.1016/j.ijbiomac.2019.09.007

  48. Li W, Zhang K, Yang H. Pectin alleviates high fat (lard) diet-induced nonalcoholic fatty liver disease in mice: possible role of short-chain fatty acids and gut microbiota regulated by pectin. J Agric Food Chem 2018; 66(30): 8015–25. doi: 10.1021/acs.jafc.8b02979

  49. Zheng J, Shen N, Wang S, Zhao G. Oat beta-glucan ameliorates insulin resistance in mice fed on high-fat and high-fructose diet. Food Nutr Res 2013; 57(1): 22754. doi: 10.3402/fnr.v57i0.22754

  50. Zhu F. Chemical composition and health effects of Tartary buckwheat. Food Chem 2016; 203: 231–45. doi: 10.1016/j.foodchem.2016.02.050

  51. Peng L, Zhang Q, Zhang Y, Yao Z, Song P, Wei L, et al. Effect of tartary buckwheat, rutin, and quercetin on lipid metabolism in rats during high dietary fat intake. Food Sci Nutr 2020; 8(1): 199–213. doi: 10.1002/fsn3.1291

  52. Seo S, Lee M-S, Chang E, Shin Y, Oh S, Kim I-H, et al. Rutin increases muscle mitochondrial biogenesis with AMPK activation in high-fat diet-induced obese rats. Nutrients 2015; 7(9): 8152–69. doi: 10.3390/nu7095385

  53. Zhou X-L, Yan B-B, Xiao Y, Zhou Y-M, Liu T-Y. Tartary buckwheat protein prevented dyslipidemia in high-fat diet-fed mice associated with gut microbiota changes. Food Chem Toxicol 2018; 119: 296–301. doi: 10.1016/j.fct.2018.02.052

  54. Muralikrishna G, Subba Rao M. Cereal non-cellulosic polysaccharides: structure and function relationship – an overview. Crit Rev Food Sci Nutr 2007; 47(6): 599–610. doi: 10.1080/10408390600919056

Published
2021-01-08
How to Cite
Wu W., Li Z., Qin F., & Qiu J. (2021). Anti-diabetic effects of the soluble dietary fiber from tartary buckwheat bran in diabetic mice and their potential mechanisms. Food & Nutrition Research, 65. https://doi.org/10.29219/fnr.v65.4998
Issue
Vol 65 (2021)
Section
Original Articles
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