White sweet potato ameliorates hyperglycemia and regenerates pancreatic islets in diabetic mice

  • Chun-Kuang Shih School of Nutrition and Health Sciences, College of Nutrition, Taipei Medical University https://orcid.org/0000-0003-2545-911X
  • Chiao-Ming Chen Department of Food Science, Nutrition, and Nutraceutical Biotechnology, Shih Chien University
  • Viola Varga School of Nutrition and Health Sciences, College of Nutrition, Taipei Medical University
  • Liang-Chen Shih School of Nutrition and Health Sciences, College of Nutrition, Taipei Medical University
  • Peng-Ru Chen Department of Food Science, Nutrition, and Nutraceutical Biotechnology, Shih Chien University
  • Shu-Fang Lo Department of Agronomy, Chiayi Agricultural Experiment Station, Taiwan Agricultural Research Institute
  • Lie-Fen Shyur Agricultural Biotechnology Research Center, Academia Sinica
  • Sing-Chung Li School of Nutrition and Health Sciences, College of Nutrition, Taipei Medical University https://orcid.org/0000-0003-4244-7911
Keywords: white sweet potato; antidiabetic; anti-hyperglycemic; pancreatic islets; insulin sensitivity

Abstract

Background: White sweet potato (WSP) has many potential beneficial effects on metabolic control and on diabetes- related insulin resistance. The antihyperglycemic effects of Tainung No. 10 (TNG10), a variety of WSP in Taiwan, warrant investigation.

Objective: To investigate the antidiabetic activity of WSP (Ipomoea batatas L. TNG10) and the mechanisms for interventions using whole leaves or tubers of WSP in diabetic mice.

Design: Mice were co-administered with streptozotocin and nicotinamide to induce diabetes and then treated with an experimental diet including either 10% WSP tuber (10%-T) and 30% WSP tuber (30%-T) or 0.5% WSP leaf (0.5%-L) and 5% WSP leaf (5%-L). After 8 weeks’ treatment, their plasma glycemic parameters, lipid profiles, and inflammatory marker were analyzed. Their pancreases were removed for histopathologic image analysis; proteins were also extracted from their muscles for phosphoinositide 3-kinase pathway analysis.

Results: The 30%-T or 5%-L mice had lower plasma glucose, insulin, glucose area under the curve (AUC), homeostatic model assessment of insulin resistance (HOMA-IR), alanine transaminase, triglyceride, and tumor necrosis factor alpha levels. In all diabetic mice, their Langerhans’s area was reduced by 60%; however, after 30% WSP-T or 5% WSP-L diets, the mice demonstrated significant restoration of the Langerhans’s areas (approximately 30%). Only in 5%-L mice, slightly increased expression of insulin-signaling pathway-related proteins, phosphorylated insulin receptor and protein kinase B and membrane glucose transporter 4 was noted.

Conclusions: WSP has antihyperglycemic effects by inducing pancreatic islet regeneration and insulin resistance amelioration. Therefore, WSP has potential applications in dietary diabetes management.

Downloads

Download data is not yet available.

References


  1. Zimmet P, Alberti KG, Magliano DJ, Bennett PH. Diabetes mellitus statistics on prevalence and mortality: facts and fallacies. Nat Rev Endocrinol 2016; 12: 616. doi: 10.1038/nrendo.2016.105.

  2. Ogurtsova K, da Rocha Fernandes JD, Huang Y, Linnenkamp U, Guariguata L, Cho NH, et al. IDF Diabetes Atlas: global estimates for the prevalence of diabetes for 2015 and 2040. Diabetes Res Clin Pract 2017; 128: 40–50. doi: 10.1016/j.diabres.2017.03.024.

  3. Shulman GI. Cellular mechanisms of insulin resistance. J Clin Investig 2000; 106(2): 171–6. doi: 10.1172/JCI10583.

  4. Kahn SE, Hull RL, Utzschneider KM. Mechanisms linking obesity to insulin resistance and type 2 diabetes. Nature 2006; 444(7121): 840. doi: 10.1038/nature05482.

  5. Hales CN, Barker DJJD. Type 2 (non-insulin-dependent) diabetes mellitus: the thrifty phenotype hypothesis. Diabetologia 1992; 35(7): 595–601. doi: 10.1093/ije/dyt133.

  6. Leibowitz G, Kaiser N, Cerasi E. β-Cell failure in type 2 diabetes. J Diabetes Investig 2011; 2(2): 82–91. doi: 10.1111/j.2040-1124.2010.00094.x.

  7. Szkudelski TJEb, medicine. Streptozotocin–nicotinamide-induced diabetes in the rat. Characteristics of the experimental model. Exp Biol Med 2012; 237(5): 481–90. doi: 10.1258/ebm.2012.011372.

  8. Masiello P, Broca C, Gross R, Roye M, Manteghetti M, Hillaire-Buys D, et al. Experimental NIDDM: development of a new model in adult rats administered streptozotocin and nicotinamide. Diabetes 1998; 47(2): 224–9. doi: 10.2337/diab.47.2.224.

  9. Nakamura T, Terajima T, Ogata T, Ueno K, Hashimoto N, Ono K, et al. Establishment and pathophysiological characterization of type 2 diabetic mouse model produced by streptozotocin and nicotinamide. Biol Pharm Bull 2006; 29(6): 1167–74. doi: 10.1248/bpb.29.1167.

  10. Huang X, Liu G, Guo J, Su Z. The PI3K/AKT pathway in obesity and type 2 diabetes. Int J Biol Sci 2018; 14(11): 1483. doi: 10.7150/ijbs.27173.

  11. Minokoshi Y, Kahn CR, Kahn BB. Tissue-specific ablation of the GLUT4 glucose transporter or the insulin receptor challenges assumptions about insulin action and glucose homeostasis. J Biol Chem 2003; 278(36): 33609–12. doi: 10.1074/jbc.R300019200.

  12. Costa MM, Violato NM, Taboga SR, Góes RM, Bosqueiro JR. Reduction of insulin signalling pathway IRS-1/IRS-2/AKT/mTOR and decrease of epithelial cell proliferation in the prostate of glucocorticoid-treated rats. Int J Exp Pathol 2012; 93(3): 188–95. doi: 10.1111/j.1365-2613.2012.00817.x.

  13. Copps K, White M. Regulation of insulin sensitivity by serine/threonine phosphorylation of insulin receptor substrate proteins IRS1 and IRS2. Diabetologia 2012; 55(10): 2565–82. doi: 10.1007/s00125-012-2644-8.

  14. Govers R. Cellular regulation of glucose uptake by glucose transporter GLUT4. Adv Clin Chem 2014; 66: 173–240. doi: 10.1016/B978-0-12-801401-1.00006-2.

  15. Saltiel AR, Kahn CR. Insulin signalling and the regulation of glucose and lipid metabolism. Nature 2001; 414: 799. doi: 10.1038/414799a.

  16. Ishiki M, Klip A. Minireview: recent developments in the regulation of glucose transporter-4 traffic: new signals, locations, and partners. Endocrinology 2005; 146(12): 5071–8. doi: 10.1210/en.2005-0850.

  17. Naowaboot J, Pannangpetch P, Kukongviriyapan V, Prawan A, Kukongviriyapan U, Itharat A. Mulberry leaf extract stimulates glucose uptake and GLUT4 translocation in rat adipocytes. Am J Chin Med 2012; 40(01): 163–75. doi: 10.1142/S0192415X12500139.

  18. Hsu CY, Shih HY, Chia YC, Lee CH, Ashida H, Lai YK, et al. Rutin potentiates insulin receptor kinase to enhance insulin-dependent glucose transporter 4 translocation. Mol Nutr Food Res 2014; 58(6): 1168–76. doi: 10.1002/mnfr.201300691.

  19. Zhang Y, Liu X, Han L, Gao X, Liu E, Wang T. Regulation of lipid and glucose homeostasis by mango tree leaf extract is mediated by AMPK and PI3K/AKT signaling pathways. Food Chem 2013; 141(3): 2896–905. doi: 10.1016/j.foodchem.2013.05.121.

  20. Ying C, Mao Y, Chen L, Wang S, Ling H, Li W, et al. Bamboo leaf extract ameliorates diabetic nephropathy through activating the AKT signaling pathway in rats. Int J Biol Macromol 2017; 105: 1587–94. doi: 10.1016/j.ijbiomac.2017.03.124.

  21. Moch. Saiful B, Hye won J, Jongwon C, Jong-Ok P. Protective effect of white-skinned sweet potato (Ipomoea batatas L.) from Indonesia on streptozotocin-induced oxidative stress in rats. J Life Sci 2010; 20(11): 1569–76. doi: 10.5352/JLS.2010.20.11.1569.

  22. Kusano S, Abe H, Tamura H. Isolation of antidiabetic components from white-skinned sweet potato (Ipomoea batatas L.). Biosci Biotechnol Biochem 2001; 65(1): 109–14. doi: 10.1271/bbb.65.109.

  23. Kusano S, Abe H. Antidiabetic activity of white skinned sweet potato (Ipomoea batatas L.) in obese Zucker fatty rats. Biol Pharm Bull 2000; 23(1): 23–6. doi: 10.1248/bpb.23.23.

  24. Oki N, Nonaka S, Ozaki S. The effects of an arabinogalactan-protein from the white-skinned sweet potato (Ipomoea batatas L.) on blood glucose in spontaneous diabetic mice. Biosci Biotechnol Biochem 2011; 75(3): 596–8. doi: 10.1271/bbb.100711.

  25. Kusano S, Tamasu S, Nakatsugawa S. Effects of the white-skinned sweet potato (Ipomoea batatas L.) on the expression of adipocytokine in adipose tissue of genetic type 2 diabetic mice. Food Sci Technol Res 2005; 11(4): 369–72. doi: 10.3136/fstr.11.369.

  26. Ludvik B, Hanefeld M, Pacini G. Improved metabolic control by Ipomoea batatas (Caiapo) is associated with increased adiponectin and decreased fibrinogen levels in type 2 diabetic subjects. Diabetes Obes Metab 2008; 10(7): 586–92. doi: 10.1111/j.1463-1326.2007.00752.x.

  27. Ludvik B, Waldhäusl W, Prager R, Kautzky-Willer A, Pacini G. Mode of action of Ipomoea batatas (Caiapo) in type 2 diabetic patients. Metabolism 2003; 52(7): 875–80. doi: 10.1016/S0026-0495(03)00073-8.

  28. Ludvik BH, Mahdjoobian K, Waldhaeusl W, Hofer A, Prager R, Kautzky-Willer A, et al. The effect of Ipomoea batatas (Caiapo) on glucose metabolism and serum cholesterol in patients with type 2 diabetes: a randomized study. Diabetes Care 2002; 25(1): 239–40. doi: 10.2337/diacare.25.1.239.

  29. Shih CK, Chen CM, Hsiao TJ, Liu CW, Li SC. White sweet potato as meal replacement for overweight white-collar workers: a randomized controlled trial. J Nutrients 2019; 11(1): 165. doi: 10.3390/nu11010165.

  30. Chen C-M, Shih C-K, Su Y-J, Cheang K-U, Lo S-F, Li S-C. Evaluation of white sweet potato tube-feeding formula in elderly diabetic patients: a randomized controlled trial. Nutr Metab 2019; 16(1): 70. doi: 10.1186/s12986-019-0398-8.

  31. Reeves PG, Nielsen FH, Fahey GC, Jr. AIN-93 Purified diets for laboratory rodents: final report of the American Institute of Nutrition Ad Hoc Writing Committee on the Reformulation of the AIN-76A Rodent Diet. Nutr 1993; 123(11): 1939–51. doi: 10.1093/jn/123.11.1939.

  32. Shimizu R, Sakazaki F, Okuno T, Nakamuro K, Ueno H. Difference in glucose intolerance between C57BL/6J and ICR strain mice with streptozotocin/nicotinamide-induced diabetes. Biomed Res 2012; 33(1): 63–6. doi: 10.2220/biomedres.33.63.

  33. Christensen SD, Mikkelsen L, Fels J, Bodvarsdottir T, Hansen A. Quality of plasma sampled by different methods for multiple blood sampling in mice. Lab Anim 2009; 43(1): 65–71. doi: 10.1258/la.2008.007075.

  34. Lee B, Shi L, Kassel DB, Asakawa T, Takeuchi K, Christopher RJ. Pharmacokinetic, pharmacodynamic, and efficacy profiles of alogliptin, a novel inhibitor of dipeptidyl peptidase-4, in rats, dogs, and monkeys. Eur J Pharmacol 2008; 589(1–3):306–14. doi: 10.1016/j.ejphar.2008.04.047.

  35. Cha DR, Zhang X, Zhang Y, Wu J, Su D, Han JY, et al. Peroxisome proliferator–activated receptor α/γ dual agonist tesaglitazar attenuates diabetic nephropathy in db/db mice. Diabetes 2007; 56(8): 2036–45. doi: 10.2337/db06-1134.

  36. Mohanraj R, Sivasankar S. Sweet potato (Ipomoea batatas [L.] Lam) – a valuable medicinal food: a review. J Med Food 2014; 17(7): 733–41. doi: 10.1089/jmf.2013.2818.

  37. Ayeleso TB, Ramachela K, Mukwevho E. A review of therapeutic potentials of sweet potato: pharmacological activities and influence of the cultivar. Trop J Pharm Res 2016; 15(12): 2751–61. doi: 10.4314/tjpr.v15i12.31.

  38. Lencioni C, Lupi R, Del Prato SJCdr. β-cell failure in type 2 diabetes mellitus. Curr Diabetes Rep 2008; 8(3): 179–84. doi: 10.1007/s11892-008-0031-0.

  39. Prentki M, Nolan CJJTJoci. Islet β cell failure in type 2 diabetes. J Clin Investig 2006; 116(7): 1802–12. doi: 10.1172/JCI29103.

  40. Sunarti, Susilowati R, Royhan A . Effects of white-skinned sweet potato (Ipomoea batatas L.) on pancreatic beta cells and insulin expression in streptozotocin induced diabetic rats. Majalah Kesehatan Pharmamedika 2009; 1(2): 45–9. https://www.researchgate.net/publication/267987188.

  41. Musilová J, Bystrická J, Árvay J, Harangózo LJP. Polyphenols and phenolic acids in sweet potato (Ipomoea batatas L.) roots. Slovak J Food Sci 2017; 11(1): 82–7. doi: 10.5219/705.

  42. Song E-K, Hur H, Han M-K. Epigallocatechin gallate prevents autoimmune diabetes induced by multiple low doses of streptozotocin in mice. Archiv Pharm Res 2003; 26(7): 559–63. doi: 10.1007/BF02976881.

  43. Bansal P, Paul P, Mudgal J, Nayak PG, Pannakal ST, Priyadarsini KI, et al. Antidiabetic, antihyperlipidemic and antioxidant effects of the flavonoid rich fraction of Pilea microphylla (L.) in high-fat diet/streptozotocin-induced diabetes in mice. Exp Toxicol Pathol 2012; 64(6): 651–8. doi: 10.1016/j.etp.2010.12.009.

  44. Bae U-J, Jung E-S, Jung S-J, Chae S-W, Park B-H. Mulberry leaf extract displays antidiabetic activity in db/db mice via Akt and AMP-activated protein kinase phosphorylation. Food Nutr Res 2018; 62: 1473. doi: 10.29219/fnr.v62.1473.

  45. Vareda PMP, Saldanha LL, Camaforte NAdP, Violato NM, Dokkedal AL, Bosqueiro JR, et al. Myrcia bella leaf extract presents hypoglycemic activity via PI3k/Akt insulin signaling pathway. Evid Based Complement Alternat Med 2014; 2014: 543606. doi: 10.1155/2014/543606.

  46. Robertson MD. Dietary-resistant starch and glucose metabolism. Curr Opin Clin Nutr Metab Care 2012; 15(4): 362–7. doi: 10.1097/MCO.0b013e3283536931.

Published
2020-03-02
How to Cite
1.
Shih C-K, Chen C-M, Varga V, Shih L-C, Chen P-R, Lo S-F, Shyur L-F, Li S-C. White sweet potato ameliorates hyperglycemia and regenerates pancreatic islets in diabetic mice. fnr [Internet]. 2020Mar.2 [cited 2020Mar.28];64. Available from: https://foodandnutritionresearch.net/index.php/fnr/article/view/3609
Section
Original Articles