Nutrition Research and Practice

The Korean Nutrition Society (한국영양학회)
권호 표지
DOI QR코드

DOI QR Code

Anti-diabetic effects of blue honeyberry on high-fed-diet-induced type II diabetic mouse

  • Sharma, Anshul (Department of Food and Nutrition, College of BioNano Technology, Gachon University) ;
  • Kim, Joo Wan (Aribio Co. Ltd.) ;
  • Ku, Sae-Kwang (Department of Anatomy and Histology, College of Korean Medicine, Daegu Haany University) ;
  • Choi, Jae-Suk (Major in Food Biotechnology, Division of Bioindustry, College of Medical and Life Sciences, Silla University) ;
  • Lee, Hae-Jeung (Department of Food and Nutrition, College of BioNano Technology, Gachon University)
  • Received : 2018.10.10
  • Accepted : 2019.04.02
  • Published : 2019.10.01
Download PDF
⟨ Previous Next ⟩

Abstract

BACKGROUND/OBJECTIVE: The blue honeysuckle berry (Lonicera caerulea var. edulis L.) is a small deciduous shrub belonging to the Caprifoliaceae family that is native to Russia, China, Japan, and Korea. The berry of this shrub is edible, sweet and juicy and is commonly known as the blue honeyberry (BHB). This study examined the anti-diabetic potential of BHB on high-fat-diet-induced mild diabetic mice. The hypoglycemic, and nephroprotective effects of the 12-week oral administration of blue honeyberry extract were analyzed. MATERIALS/METHODS: The hypoglycemic effects were based on the observed changes in insulin, blood glucose, and glycated hemoglobin (HbA1c). Furthermore, the changes in the weight of the pancreas, including its histopathology and immunohistochemical investigation were also performed. Moreover, the nephroprotective effects were analyzed by observing the changes in kidney weight, its histopathology, blood urea nitrogen (BUN), and serum creatinine levels. RESULTS: The results showed that the high-fat diet (HFD)-induced control mice showed a noticeable increase in blood glucose, insulin, HbA1c, BUN, and creatinine levels. Furthermore, growth was observed in lipid droplet deposition related to the degenerative lesions in the vacuolated renal tubules with the evident enlargement and hyperplasia of the pancreatic islets. In addition, in the endocrine pancreas, there was an increase in the insulin-and glucagon-producing cells, as well as in the insulin/glucagon cell ratios. On the other hand, compared to the HFD-treated mice group, all these diabetic and related complications were ameliorated significantly in a dose-dependent manner after 84 days of the continuous oral administration of BHBe at 400, 200 and 100 mg/kg, and a dramatic resettlement in the hepatic glucose-regulating enzyme activities was observed. CONCLUSIONS: By assessing the key parameters for T2DM, the present study showed that the BHBe could act as a potential herbal agent to cure diabetes (type II) and associated ailments in HFD-induced mice.

Keywords

References

  1. Cho NH, Shaw JE, Karuranga S, Huang Y, da Rocha Fernandes JD, Ohlrogge AW, Malanda B. IDF Diabetes Atlas: global estimates of diabetes prevalence for 2017 and projections for 2045. Diabetes Res Clin Pract 2018;138:271-281. https://doi.org/10.1016/j.diabres.2018.02.023
  2. Sami W, Ansari T, Butt NS, Hamid MRA. Effect of diet on type 2 diabetes mellitus: a review. Int J Health Sci (Qassim) 2017;11:65-71.
  3. Enk J, Mandelboim O. The role of natural cytotoxicity receptors in various pathologies: emphasis on type I diabetes. Front Immunol 2014;5:4. https://doi.org/10.3389/fimmu.2014.00004
  4. Kolluru GK, Bir SC, Kevil CG. Endothelial dysfunction and diabetes: effects on angiogenesis, vascular remodeling, and wound healing. Int J Vasc Med 2012;2012:918267. https://doi.org/10.1155/2012/918267
  5. Kahn SE, Cooper ME, Del Prato S. Pathophysiology and treatment of type 2 diabetes: perspectives on the past, present, and future. Lancet 2014;383:1068-1083. https://doi.org/10.1016/S0140-6736(13)62154-6
  6. Wright JJ, Tylee TS. Pharmacologic therapy of type 2 diabetes. Med Clin North Am 2016;100:647-663. https://doi.org/10.1016/j.mcna.2016.03.014
  7. Lotfy M, Adeghate J, Kalasz H, Singh J, Adeghate E. Chronic complications of diabetes mellitus: a mini review. Curr Diabetes Rev 2017;13:3-10.
  8. Lindstrom J, Peltonen M, Eriksson JG, Ilanne-Parikka P, Aunola S, Keinanen-Kiukaanniemi S, Uusitupa M, Tuomilehto J; Finnish Diabetes Prevention Study (DPS). Improved lifestyle and decreased diabetes risk over 13 years: long-term follow-up of the randomised Finnish Diabetes Prevention Study (DPS). Diabetologia 2013;56:284-293. https://doi.org/10.1007/s00125-012-2752-5
  9. Shah P, Mudaliar S. Pioglitazone: side effect and safety profile. Expert Opin Drug Saf 2010;9:347-354. https://doi.org/10.1517/14740331003623218
  10. Kang SJ, Lee JE, Lee EK, Jung DH, Song CH, Park SJ, Choi SH, Han CH, Ku SK, Lee YJ. Fermentation with Aquilariae lignum enhances the anti-diabetic activity of green tea in type II diabetic db/db mouse. Nutrients 2014;6:3536-3571. https://doi.org/10.3390/nu6093536
  11. Mottillo EP, Desjardins EM, Fritzen AM, Zou VZ, Crane JD, Yabut JM, Kiens B, Erion DM, Lanba A, Granneman JG, Talukdar S, Steinberg GR. FGF21 does not require adipocyte AMP-activated protein kinase (AMPK) or the phosphorylation of acetyl-CoA carboxylase (ACC) to mediate improvements in whole-body glucose homeostasis. Mol Metab 2017;6:471-481. https://doi.org/10.1016/j.molmet.2017.04.001
  12. Ma A, Wang J, Yang L, An Y, Zhu H. AMPK activation enhances the anti-atherogenic effects of high density lipoproteins in apo$E^{-/-}$ mice. J Lipid Res 2017;58:1536-1547. https://doi.org/10.1194/jlr.M073270
  13. Out M, Kooy A, Lehert P, Schalkwijk CA, Stehouwer CDA. Long-term treatment with metformin in type 2 diabetes and methylmalonic acid: Post hoc analysis of a randomized controlled 4.3year trial. J Diabetes Complications 2018;32:171-178. https://doi.org/10.1016/j.jdiacomp.2017.11.001
  14. Zdilla MJ. Metformin with either histamine H2-receptor antagonists or proton pump inhibitors: A polypharmacy recipe for neuropathy via vitamin B12 depletion. Clin Diabetes 2015;33:90-95. https://doi.org/10.2337/diaclin.33.2.90
  15. Khurana R, Malik IS. Metformin: safety in cardiac patients. Heart 2010;96:99-102.
  16. Chaovanalikit A, Thompson MM, Wrolstad RE. Characterization and quantification of anthocyanins and polyphenolics in blue honeysuckle (Lonicera caerulea L.). J Agric Food Chem 2004;52:848-852. https://doi.org/10.1021/jf030509o
  17. Svarcova I, Heinrich J, Valentova K. Berry fruits as a source of biologically active compounds: the case of Lonicera caerulea. Biomed Pap Med Fac Univ Palacky Olomouc Czech Repub 2007;151:163-174. https://doi.org/10.5507/bp.2007.031
  18. Liu S, Xu Q, Li X, Wang Y, Zhu J, Ning C, Chang X, Meng X. Effects of high hydrostatic pressure on physicochemical properties, enzymes activity, and antioxidant capacities of anthocyanins extracts of wild Lonicera caerulea berry. Innov Food Sci Emerg Technol 2016;36:48-58. https://doi.org/10.1016/j.ifset.2016.06.001
  19. Oszmianski J, Wojdylo A, Lachowicz S. Effect of dried powder preparation process on polyphenolic content and antioxidant activity of blue honeysuckle berries (Lonicera caerulea L. var. kamtschatica). LWT-Food Sci Technol 2016;67:214-222. https://doi.org/10.1016/j.lwt.2015.11.051
  20. Becker R, Paczkowski C, Szakiel A. Triterpenoid profile of fruit and leaf cuticular waxes of edible honeysuckle Lonicera caerulea var. kamtschatica. Acta Soc Bot Pol 2017;86:3539.
  21. Chen L, Xin X, Yuan Q, Su D, Liu W. Phytochemical properties and antioxidant capacities of various colored berries. J Sci Food Agric 2014;94:180-188. https://doi.org/10.1002/jsfa.6216
  22. Zhao H, Wang Z, Ma F, Yang X, Cheng C, Yao L. Protective effect of anthocyanin from Lonicera caerulea var. edulis on radiationinduced damage in mice. Int J Mol Sci 2012;13:11773-11782. https://doi.org/10.3390/ijms130911773
  23. Palikova I, Valentova K, Oborna I, Ulrichova J. Protectivity of blue honeysuckle extract against oxidative human endothelial cells and rat hepatocyte damage. J Agric Food Chem 2009;57:6584-6589. https://doi.org/10.1021/jf9003994
  24. Vostalova J, Galandakova A, Palikova I, Ulrichova J, Dolezal D, Lichnovska R, Vrbkova J, Rajnochova SA. Lonicera caerulea fruits reduce UVA-induced damage in hairless mice. J Photochem Photobiol B 2013;128:1-11. https://doi.org/10.1016/j.jphotobiol.2013.07.024
  25. Wu D, Zheng N, Qi K, Cheng H, Sun Z, Gao B, Zhang Y, Pang W, Huangfu C, Ji S, Xue M, Ji A, Li Y. Exogenous hydrogen sulfide mitigates the fatty liver in obese mice through improving lipid metabolism and antioxidant potential. Med Gas Res 2015;5:1. https://doi.org/10.1186/s13618-014-0022-y
  26. Park SI, Lee YJ, Choi SH, Park SJ, Song CH, Ku SK. Therapeutic effects of blue honeysuckle on lesions of hyperthyroidism in rats. Am J Chin Med 2016;44:1441-1456. https://doi.org/10.1142/S0192415X16500804
  27. Jurgonski A, Juskiewicz J, Zdunczyk Z. An anthocyanin-rich extract from Kamchatka honeysuckle increases enzymatic activity within the gut and ameliorates abnormal lipid and glucose metabolism in rats. Nutrition 2013;29:898-902. https://doi.org/10.1016/j.nut.2012.11.006
  28. Wu S, He X, Wu X, Qin S, He J, Zhang S, Hou DX. Inhibitory effects of blue honeysuckle (Lonicera caerulea L) on adjuvant-induced arthritis in rats: crosstalk of anti-inflammatory and antioxidant effects. J Funct Foods 2015;17:514-523. https://doi.org/10.1016/j.jff.2015.06.007
  29. Zhao J, Lin Y, Zhao Y, Wang Y, Ning C, Ma Y, Meng X. Polyphenolrich blue honeysuckle extract alleviates silica particle-induced inflammatory responses and macrophage apoptosis via NRF2/HO-1 and MAPK signaling. J Funct Foods 2018;46:463-474. https://doi.org/10.1016/j.jff.2018.05.024
  30. Liu S, You L, Zhao Y, Chang X. Wild Lonicera caerulea berry polyphenol extract reduces cholesterol accumulation and enhances antioxidant capacity in vitro and in vivo. Food Res Int 2018;107:73-83. https://doi.org/10.1016/j.foodres.2018.02.016
  31. Liu S, Wu Z, Guo S, Meng X, Chang X. Polyphenol-rich extract from wild Lonicera caerulea berry reduces cholesterol accumulation by mediating the expression of hepatic miR-33 and miR-122, HMGCR, and CYP7A1 in rats. J Funct Foods 2018;40:648-658. https://doi.org/10.1016/j.jff.2017.11.048
  32. Liu M, Tan J, He Z, He X, Hou DX, He J, Wu S. Inhibitory effect of blue honeysuckle extract on high-fat-diet-induced fatty liver in mice. Anim Nutr 2018;4:288-293. https://doi.org/10.1016/j.aninu.2018.06.001
  33. Lee HS, Chang JH, Ku SK. An immunohistochemical study of the pancreatic endocrine cells of the ddN mouse. Folia Histochem Cytobiol 2010;48: 387-393.
  34. Lee JE, Kang SJ, Choi SH, Song CH, Lee YJ, Ku SK. Fermentation of green tea with 2% Aquilariae lignum increases the anti-diabetic activity of green tea aqueous extracts in the high fat-fed mouse. Nutrients 2015;7:9046-9078. https://doi.org/10.3390/nu7115447
  35. Lee HS, Chang JH, Ku SK. An immunohistochemical study of the pancreatic endocrine cells of the ddN mouse. Folia Histochem Cytobiol 2010;48:387-393.
  36. Levene A. Pathological factors influencing excision of tumours in the head and neck. Part I. Clin Otolaryngol Allied Sci 1981;6:145-151. https://doi.org/10.1111/j.1365-2273.1981.tb01800.x
  37. Ludbrook J. Update: microcomputer statistics packages. A personal view. Clin Exp Pharmacol Physiol 1997;24:294-296. https://doi.org/10.1111/j.1440-1681.1997.tb01823.x
  38. Choi JS, Kim JW, Park JB, Pyo SE, Hong YK, Ku SK, Kim MR. Blood glycemia-modulating effects of melanian snail protein hydrolysates in mice with type II diabetes. Int J Mol Med 2017;39:1437-1451. https://doi.org/10.3892/ijmm.2017.2967
  39. Jurikova T, Rop O, Mlcek J, Sochor J, Balla S, Szekeres L, Hegedusova A, Hubalek J, Adam V, Kizek R. Phenolic profile of edible honeysuckle berries (Genus Lonicera) and their biological effects. Molecules 2012;17:61-79. https://doi.org/10.3390/molecules17010061
  40. Rupasinghe HPV, Arumuggam N, Amararathna M, De Silva ABKH. The potential health benefits of haskap (Lonicera caerulea L.): role of cyanidin-3-O-glucoside. J Funct Foods 2018;44:24-39. https://doi.org/10.1016/j.jff.2018.02.023
  41. Sancho RAS, Pastore GM. Evaluation of the effects of anthocyanins in type 2 diabetes. Food Res Int 2012;46:378-386. https://doi.org/10.1016/j.foodres.2011.11.021
  42. Podsedek A, Majewska I, Redzynia M, Sosnowska D, Koziolkiewicz M. In vitro inhibitory effect on digestive enzymes and antioxidant potential of commonly consumed fruits. J Agric Food Chem 2014;62:4610-4617. https://doi.org/10.1021/jf5008264
  43. Tan Y, Kim J, Cheng J, Ong M, Lao WG, Jin XL, Lin YG, Xiao L, Zhu XQ, Qu XQ. Green tea polyphenols ameliorate non-alcoholic fatty liver disease through upregulating AMPK activation in high fat fed Zucker fatty rats. World J Gastroenterol 2017;23:3805-3814. https://doi.org/10.3748/wjg.v23.i21.3805
  44. Kim UH, Yoon JH, Li H, Kang JH, Ji HS, Park KH, Shin DH, Park HY, Jeong TS. Pterocarpan-enriched soy leaf extract ameliorates insulin sensitivity and pancreatic $\beta$-cell proliferation in type 2 diabetic mice. Molecules 2014;19:18493-18510. https://doi.org/10.3390/molecules191118493
  45. Samuel VT, Liu ZX, Qu X, Elder BD, Bilz S, Befroy D, Romanelli AJ, Shulman GI. Mechanism of hepatic insulin resistance in nonalcoholic fatty liver disease. J Biol Chem 2004;279:32345-32353. https://doi.org/10.1074/jbc.M313478200
  46. Savage DB, Petersen KF, Shulman GI. Disordered lipid metabolism and the pathogenesis of insulin resistance. Physiol Rev 2007;87:507-520. https://doi.org/10.1152/physrev.00024.2006
  47. Chen H, Qu Z, Fu L, Dong P, Zhang X. Physicochemical properties and antioxidant capacity of 3 polysaccharides from green tea, oolong tea, and black tea. J Food Sci 2009;74:C469-C474. https://doi.org/10.1111/j.1750-3841.2009.01231.x
  48. Ku SK, Sung SH, Choung JJ, Choi JS, Shin YK, Kim JW. Anti-obesity and anti-diabetic effects of a standardized potato extract in ob/ob mice. Exp Ther Med 2016;12:354-364. https://doi.org/10.3892/etm.2016.3256
  49. Lo HY, Hsiang CY, Li TC, Li CC, Huang HC, Chen JC, Ho TY. A novel glycated hemoglobin A1c-lowering traditional Chinese medicinal formula, identified by translational medicine study. PLoS One 2014;9:e104650. https://doi.org/10.1371/journal.pone.0104650
  50. Zhang X, Gregg EW, Williamson DF, Barker LE, Thomas W, Bullard KM, Imperatore G, Williams DE, Albright AL. A1C level and future risk of diabetes: a systematic review. Diabetes Care 2010;33:1665-1673. https://doi.org/10.2337/dc09-1939
  51. Kim CM, Yi SJ, Cho IJ, Ku SK. Red-koji fermented red ginseng ameliorates high fat diet-induced metabolic disorders in mice. Nutrients 2013;5:4316-4332. https://doi.org/10.3390/nu5114316
  52. Chung SI, Rico CW, Kang MY. Comparative study on the hypoglycemic and antioxidative effects of fermented paste (doenjang) prepared from soybean and brown rice mixed with rice bran or red ginseng marc in mice fed with high fat diet. Nutrients 2014;6:4610-4624. https://doi.org/10.3390/nu6104610
  53. Terauchi Y, Takamoto I, Kubota N, Matsui J, Suzuki R, Komeda K, Hara A, Toyoda Y, Miwa I, Aizawa S, Tsutsumi S, Tsubamoto Y, Hashimoto S, Eto K, Nakamura A, Noda M, Tobe K, Aburatani H, Nagai R, Kadowaki T. Glucokinase and IRS-2 are required for compensatory beta cell hyperplasia in response to high-fat diet-induced insulin resistance. J Clin Invest 2007;117:246-257. https://doi.org/10.1172/JCI17645
  54. Noriega-Lopez L, Tovar AR, Gonzalez-Granillo M, Hernandez-Pando R, Escalante B, Santillan-Doherty P, Torres N. Pancreatic insulin secretion in rats fed a soy protein high fat diet depends on the interaction between the amino acid pattern and isoflavones. J Biol Chem 2007;282:20657-20666. https://doi.org/10.1074/jbc.M701045200

Cited by

  1. Lonicera caerulea: An updated account of its phytoconstituents and health-promoting activities vol.107, 2021, https://doi.org/10.1016/j.tifs.2020.08.013
  2. Antioxidant Effect of Lonicera caerulea L. in the Cardiovascular System of Obese Zucker Rats vol.10, pp.8, 2019, https://doi.org/10.3390/antiox10081199
  3. Recent Studies on Berry Bioactives and Their Health-Promoting Roles vol.27, pp.1, 2022, https://doi.org/10.3390/molecules27010108