DOI QR코드

DOI QR Code

Effects of cranberry powder on biomarkers of oxidative stress and glucose control in db/db mice

  • Kim, Mi Joung (Department of Food and Nutrition, College of Natural Sciences, Seoul Women's University) ;
  • Chung, Jee-Young (Department of Food and Nutrition, College of Natural Sciences, Seoul Women's University) ;
  • Kim, Jung Hee (Department of Food and Nutrition, College of Natural Sciences, Seoul Women's University) ;
  • Kwak, Ho-Kyung (Department of Home Economics, Korea National Open University)
  • Received : 2012.09.25
  • Accepted : 2013.10.02
  • Published : 2013.12.01

Abstract

Increased oxidative stress in obese diabetes may have causal effects on diabetic complications, including dyslipidemia. Lipopolysccharides (LPS) along with an atherogenic diet have been found to increase oxidative stress and insulin resistance. Cranberry has been recognized as having beneficial effects on diseases related to oxidative stress. Therefore, we employed obese diabetic animals treated with an atherogenic diet and LPS, with the aim of examining the effects of cranberry powder (CP) on diabetic related metabolic conditions, including lipid profiles, serum insulin and glucose, and biomarkers of oxidative stress. Forty C57BL/KsJ-db/db mice were divided into the following five groups: normal diet + saline, atherogenic diet + saline, atherogenic diet + LPS, atherogenic diet + 5% CP + LPS, and atherogenic diet + 10% CP + LPS. Consumption of an atherogenic diet resulted in elevation of serum total cholesterol and atherogenic index (AI) and reduction of high density lipoprotein (HDL)-cholesterol. However, with 10% CP, the increase in mean HDL-cholesterol level was close to that of the group with a normal diet, whereas AI was maintained at a higher level than that of the group with a normal diet. LPS induced elevated serum insulin level was lowered by greater than 60% with CP (P < 0.05), and mean serum glucose level was reduced by approximately 19% with 5% CP (P > 0.05). Mean activity of liver cytosolic glutathione peroxidase was significantly increased by LPS injection, however it was reduced back to the value without LPS when the diet was fortified with 10% CP (P < 0.05). In groups with CP, a reduction in mean levels of serum protein carbonyl tended to occur in a dose dependent manner. Particularly with 10% CP, a reduction of approximately 89% was observed (P > 0.05). Overall results suggest that fortification of the atherogenic diet with CP may have potential health benefits for obese diabetes with high oxidative stress, by modulation of physical conditions, including some biomarkers of oxidative stress.

Keywords

References

  1. Knekt P, Kumpulainen J, Järvinen R, Rissanen H, Heliövaara M, Reunanen A, Hakulinen T, Aromaa A. Flavonoid intake and risk of chronic diseases. Am J Clin Nutr 2002;76:560-8. https://doi.org/10.1093/ajcn/76.3.560
  2. Scalbert A, Manach C, Morand C, Remesy C, Jimenez L. Dietary polyphenols and the prevention of diseases. Crit Rev Food Sci Nutr 2005;45:287-306. https://doi.org/10.1080/1040869059096
  3. Vinson JA, Su X, Zubik L, Bose P. Phenol antioxidant quantity and quality in foods: fruits. J Agric Food Chem 2001;49:5315-21. https://doi.org/10.1021/jf0009293
  4. Liu H, Liu H, Wang W, Khoo C, Taylor J, Gu L. Cranberry phytochemicals inhibit glycation of human hemoglobin and serum albumin by scavenging reactive carbonyls. Food Funct 2011;2:475-82. https://doi.org/10.1039/c1fo10087d
  5. Gotteland M, Andrews M, Toledo M, Munoz L, Caceres P, Anziani A, Wittig E, Speisky H, Salazar G. Modulation of Helicobacter pylori colonization with cranberry juice and Lactobacillus johnsonii La1 in children. Nutrition 2008;24:421-6. https://doi.org/10.1016/j.nut.2008.01.007
  6. Ovaskainen ML, Torronen R, Koponen JM, Sinkko H, Hellström J, Reinivuo H, Mattila P. Dietary intake and major food sources of polyphenols in Finnish adults. J Nutr 2008;138:562-6. https://doi.org/10.1093/jn/138.3.562
  7. Kim MJ, Ohn J, Kim JH, Kwak HK. Effects of freeze-dried cranberry powder on serum lipids and inflammatory markers in lipopolysaccharide treated rats fed an atherogenic diet. Nutr Res Pract 2011;5:404-11. https://doi.org/10.4162/nrp.2011.5.5.404
  8. Chambers BK, Camire ME. Can cranberry supplementation benefit adults with type 2 diabetes? Diabetes Care 2003;26: 2695-6. https://doi.org/10.2337/diacare.26.9.2695
  9. Zhu M, Hu J, Perez E, Phillips D, Kim W, Ghaedian R, Napora JK, Zou S. Effects of long-term cranberry supplementation on endocrine pancreas in aging rats. J Gerontol A Biol Sci Med Sci 2011;66:1139-51.
  10. Pinto Mda S, Ghaedian R, Shinde R, Shetty K. Potential of cranberry powder for management of hyperglycemia using in vitro models. J Med Food 2010;13:1036-44. https://doi.org/10.1089/jmf.2009.0225
  11. Dandona P, Aljada A, Bandyopadhyay A. Inflammation: the link between insulin resistance, obesity and diabetes. Trends Immunol 2004;25:4-7. https://doi.org/10.1016/j.it.2003.10.013
  12. Goldberg IJ. Clinical review 124: diabetic dyslipidemia: causes and consequences. J Clin Endocrinol Metab 2001;86:965-71. https://doi.org/10.1210/jcem.86.3.7304
  13. Ihara Y, Toyokuni S, Uchida K, Odaka H, Tanaka T, Ikeda H, Hiai H, Seino Y, Yamada Y. Hyperglycemia causes oxidative stress in pancreatic beta-cells of GK rats, a model of type 2 diabetes. Diabetes 1999;48:927-32. https://doi.org/10.2337/diabetes.48.4.927
  14. Baynes JW. Role of oxidative stress in development of complications in diabetes. Diabetes 1991;40:405-12.
  15. Meng X, Tancharoen S, Kawahara KI, Nawa Y, Taniguchi S, Hashiguchi T, Maruyama I. 1,5-Anhydroglucitol attenuates cytokine release and protects mice with type 2 diabetes from inflammatory reactions. Int J Immunopathol Pharmacol 2010;23:105-19. https://doi.org/10.1177/039463201002300110
  16. Shah BR, Hux JE. Quantifying the risk of infectious diseases for people with diabetes. Diabetes Care 2003;26:510-3. https://doi.org/10.2337/diacare.26.2.510
  17. Harbuz M. Neuroendocrinology of autoimmunity. Int Rev Neurobiol 2002;52:133-61. https://doi.org/10.1016/S0074-7742(02)52008-0
  18. Kukongviriyapan U, Sompamit K, Pannangpetch P, Kukongviriyapan V, Donpunha W. Preventive and therapeutic effects of quercetin on lipopolysaccharide-induced oxidative stress and vascular dysfunction in mice. Can J Physiol Pharmacol 2012;90:1345-53. https://doi.org/10.1139/y2012-101
  19. Cani PD, Osto M, Geurts L, Everard A. Involvement of gut microbiota in the development of low-grade inflammation and type 2 diabetes associated with obesity. Gut Microbes 2012; 3:279-88. https://doi.org/10.4161/gmic.19625
  20. Cani PD, Amar J, Iglesias MA, Poggi M, Knauf C, Bastelica D, Neyrinck AM, Fava F, Tuohy KM, Chabo C, Waget A, Delmée E, Cousin B, Sulpice T, Chamontin B, Ferrières J, Tanti JF, Gibson GR, Casteilla L, Delzenne NM, Alessi MC, Burcelin R. Metabolic endotoxemia initiates obesity and insulin resistance. Diabetes 2007;56:1761-72. https://doi.org/10.2337/db06-1491
  21. Sahai A, Malladi P, Pan X, Paul R, Melin-Aldana H, Green RM, Whitington PF. Obese and diabetic db/db mice develop marked liver fibrosis in a model of nonalcoholic steatohepatitis: role of short-form leptin receptors and osteopontin. Am J Physiol Gastrointest Liver Physiol 2004;287:G1035-43. https://doi.org/10.1152/ajpgi.00199.2004
  22. Report of the American Institute of Nutrition ad hoc Committee on standards for nutritional studies. J Nutr 1977;107:1340-8. https://doi.org/10.1093/jn/107.7.1340
  23. Masmoudi A, Labourdette G, Mersel M, Huang FL, Huang KP, Vincendon G, Malviya AN. Protein kinase C located in rat liver nuclei. Partial purification and biochemical and immunochemical characterization. J Biol Chem 1989;264:1172-9.
  24. Lauer RM, Lee J, Clarke WR. Factors affecting the relationship between childhood and adult cholesterol levels: the Muscatine Study. Pediatrics 1988;82:309-18.
  25. Benzie IF, Strain JJ. The ferric reducing ability of plasma (FRAP) as a measure of "antioxidant power": the FRAP assay. Anal Biochem 1996;239:70-6. https://doi.org/10.1006/abio.1996.0292
  26. Ainsworth EA, Gillespie KM. Estimation of total phenolic content and other oxidation substrates in plant tissues using Folin-Ciocalteu reagent. Nat Protoc 2007;2:875-7. https://doi.org/10.1038/nprot.2007.102
  27. Zhishen J, Mengcheng T, Jianming W. The determination of flavonoid contents in mulberry and their scavenging effects on superoxide radicals. Food Chem 1999; 64: 555-9. https://doi.org/10.1016/S0308-8146(98)00102-2
  28. Lowry OH, Rosebrough NJ, Farr AL, Randall RJ. Protein measurement with the Folin phenol reagent. J Biol Chem 1951; 193:265-75.
  29. Kobayashi K, Forte TM, Taniguchi S, Ishida BY, Oka K, Chan L. The db/db mouse, a model for diabetic dyslipidemia: molecular characterization and effects of Western diet feeding. Metabolism 2000;49:22-31. https://doi.org/10.1016/S0026-0495(00)90588-2
  30. MacLean PS, Bower JF, Vadlamudi S, Osborne JN, Bradfield JF, Burden HW, Bensch WH, Kauffman RF, Barakat HA. Cholesteryl ester transfer protein expression prevents diet-induced atherosclerotic lesions in male db/db mice. Arterioscler Thromb Vasc Biol 2003; 23:1412-5. https://doi.org/10.1161/01.ATV.0000080687.94313.67
  31. Memon RA, Grunfeld C, Moser AH, Feingold KR. Tumor necrosis factor mediates the effects of endotoxin on cholesterol and triglyceride metabolism in mice. Endocrinology 1993;132: 2246-53. https://doi.org/10.1210/endo.132.5.8477669
  32. Wald NJ, Law MR. Serum cholesterol and ischaemic heart disease. Atherosclerosis 1995;118 Suppl:S1-5. https://doi.org/10.1016/0021-9150(95)90067-5
  33. Goldberg IJ. Lipoprotein lipase and lipolysis: central roles in lipoprotein metabolism and atherogenesis. J Lipid Res 1996;37: 693-707.
  34. Ruel G, Pomerleau S, Couture P, Lemieux S, Lamarche B, Couillard C. Favourable impact of low-calorie cranberry juice consumption on plasma HDL-cholesterol concentrations in men. Br J Nutr 2006;96:357-64. https://doi.org/10.1079/BJN20061814
  35. Kiehm TG, Anderson JW, Ward K. Beneficial effects of a high carbohydrate, high fiber diet on hyperglycemic diabetic men. Am J Clin Nutr 1976;29:895-9. https://doi.org/10.1093/ajcn/29.8.895
  36. Deyhim F, Patil BS, Villarreal A, Lopez E, Garcia K, Rios R, Garcia C, Gonzales C, Mandadi K. Cranberry juice increases antioxidant status without affecting cholesterol homeostasis in orchidectomized rats. J Med Food 2007;10:49-53. https://doi.org/10.1089/jmf.2006.218
  37. Vives-Pi M, Somoza N, Fernández-Alvarez J, Vargas F, Caro P, Alba A, Gomis R, Labeta MO, Pujol-Borrell R. Evidence of expression of endotoxin receptors CD14, toll-like receptors TLR4 and TLR2 and associated molecule MD-2 and of sensitivity to endotoxin (LPS) in islet beta cells. Clin Exp Immunol 2003;133: 208-18. https://doi.org/10.1046/j.1365-2249.2003.02211.x
  38. Jankowski A, Jankowska B, Niedworok J. The effect of anthocyanin dye from grapes on experimental diabetes. Folia Med Cracov 2000;41:5-15.
  39. Khanal RC, Rogers TJ, Wilkes SE, Howard LR, Prior RL. Effects of dietary consumption of cranberry powder on metabolic parameters in growing rats fed high fructose diets. Food Funct 2010;1:116-23. https://doi.org/10.1039/c0fo00089b
  40. Koerner A, Kratzsch J, Kiess W. Adipocytokines: leptin--the classical, resistin--the controversical, adiponectin--the promising, and more to come. Best Pract Res Clin Endocrinol Metab 2005;19:525-46. https://doi.org/10.1016/j.beem.2005.07.008
  41. Morton GJ, Gelling RW, Niswender KD, Morrison CD, Rhodes CJ, Schwartz MW. Leptin regulates insulin sensitivity via phosphatidylinositol-3-OH kinase signaling in mediobasal hypothalamic neurons. Cell Metab 2005;2:411-20. https://doi.org/10.1016/j.cmet.2005.10.009
  42. Kimura H, Ogawa S, Sugiyama A, Jisaka M, Takeuchi T, Yokota K. Anti-obesity effects of highly polymeric proanthocyanidins from seed shells of Japanese horse chestnut (Aesculus turbinata Blume). Food Res Int 2011;44:121-6. https://doi.org/10.1016/j.foodres.2010.10.052
  43. Hsu DZ, Liu MY. Sesame oil protects against lipopolysaccharidestimulated oxidative stress in rats. Crit Care Med 2004;32:227-31. https://doi.org/10.1097/01.CCM.0000104947.16669.29
  44. Ruel G, Pomerleau S, Couture P, Lamarche B, Couillard C. Changes in plasma antioxidant capacity and oxidized low-density lipoprotein levels in men after short-term cranberry juice consumption. Metabolism 2005;54:856-61. https://doi.org/10.1016/j.metabol.2005.01.031
  45. Kim JH, Kim MK. Effect of different part of mandarin intake on antioxidative capacity in 15-month-old rats. Korean J Nutr 2003;36:559-69.
  46. Zhu Y, Carvey PM, Ling Z. Altered glutathione homeostasis in animals prenatally exposed to lipopolysaccharide. Neurochem Int 2007;50:671-80. https://doi.org/10.1016/j.neuint.2006.12.013
  47. Cote J, Caillet S, Doyon G, Sylvain JF, Lacroix M. Bioactive compounds in cranberries and their biological properties. Crit Rev Food Sci Nutr 2010;50:666-79. https://doi.org/10.1080/10408390903044107
  48. Dalle-Donne I, Giustarini D, Colombo R, Rossi R, Milzani A. Protein carbonylation in human diseases. Trends Mol Med 2003; 9:169-76. https://doi.org/10.1016/S1471-4914(03)00031-5
  49. Suzuki YJ, Carini M, Butterfield DA. Protein carbonylation. Antioxid Redox Signal 2010;12:323-5. https://doi.org/10.1089/ars.2009.2887
  50. Negre-Salvayre A, Coatrieux C, Ingueneau C, Salvayre R. Advanced lipid peroxidation end products in oxidative damage to proteins. Potential role in diseases and therapeutic prospects for the inhibitors. Br J Pharmacol 2008;153:6-20. https://doi.org/10.1038/sj.bjp.0707395

Cited by

  1. Modulation of Strawberry/Cranberry Phenolic Compounds Glucuronidation by Co-Supplementation with Onion: Characterization of Phenolic Metabolites in Rat Plasma Using an Optimized μSPE–UHPLC-MS/MS Method vol.62, pp.14, 2014, https://doi.org/10.1021/jf404965z
  2. Liquid chromatography with tandem mass spectrometry quantification of urinary proanthocyanin A2 dimer and its potential use as a biomarker of cranberry intake vol.39, pp.2, 2015, https://doi.org/10.1002/jssc.201500922
  3. Antioxidant Properties of Polyphenol Fractions from Cranberry Powder in LPS-Stimulated RAW264.7 Cells vol.44, pp.8, 2015, https://doi.org/10.3746/jkfn.2015.44.8.1241
  4. Impact of Nutrients and Food Components on Dyslipidemias: What Is the Evidence? vol.6, pp.6, 2015, https://doi.org/10.3945/an.115.009480
  5. Cranberry antioxidant power on oxidative stress, inflammation and mitochondrial damage vol.21, pp.1, 2018, https://doi.org/10.1080/10942912.2017.1409758
  6. Anti-inflammatory Activity of Berry Fruits in Mice Model of Inflammation is Based on Oxidative Stress Modulation vol.8, pp.5, 2016, https://doi.org/10.4103/0974-8490.178642
  7. Impact of Cranberries on Gut Microbiota and Cardiometabolic Health: Proceedings of the Cranberry Health Research Conference 2015 vol.7, pp.4, 2013, https://doi.org/10.3945/an.116.012583
  8. A polyphenol-rich cranberry extract reverses insulin resistance and hepatic steatosis independently of body weight loss vol.6, pp.12, 2013, https://doi.org/10.1016/j.molmet.2017.10.003
  9. Cranberry Attenuates Progression of Non-alcoholic Fatty Liver Disease Induced by High-Fat Diet in Mice vol.42, pp.8, 2019, https://doi.org/10.1248/bpb.b18-00984
  10. The efficacy of berries against lipopolysaccharide-induced inflammation: A review vol.117, pp.None, 2013, https://doi.org/10.1016/j.tifs.2021.01.015