Hesperidin and naringin attenuate hyperglycemia-mediated oxidative stress and proinflammatory cytokine production in high fat fed/streptozotocin-induced type 2 diabetic rats

Journal of Diabetes and its Complications

Volumn 26, Issue 6, 2012, Pages 483-490

  Mahmoud, Ayman M ^a   Ashour, Mohamed B ^a   Abdel Moneim, Adel ^a   Ahmed, Osama M ^a  

^a Beni Suef University   (Egypt)

Author keywords

Hesperidin and naringin; HFD STZ diabetes; Lipid peroxidation; Oxidative stress; Proinflammatory cytokines

Indexed keywords

ALPHA TOCOPHEROL; ASCORBIC ACID; AURANTIIN; GLUCOSE; GLUTATHIONE; GLYCOSYLATED HEMOGLOBIN; HESPERIDIN; INSULIN; INTERLEUKIN 6; MALONALDEHYDE; NITRIC OXIDE; TUMOR NECROSIS FACTOR ALPHA;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BLOOD CHEMISTRY; CONTROLLED STUDY; CYTOKINE PRODUCTION; GLUCOSE BLOOD LEVEL; HOMEOSTASIS; HYPERGLYCEMIA; INSULIN BLOOD LEVEL; INSULIN RESISTANCE; MALE; NON INSULIN DEPENDENT DIABETES MELLITUS; NONHUMAN; OUTCOME ASSESSMENT; OXIDATIVE STRESS; PRIORITY JOURNAL; RAT;

ANIMALS; ANTI-INFLAMMATORY AGENTS, NON-STEROIDAL; ANTIOXIDANTS; CYTOKINES; DIABETES MELLITUS, TYPE 2; DIET, HIGH-FAT; DIETARY SUPPLEMENTS; FLAVANONES; GLUTATHIONE; HEMOGLOBIN A, GLYCOSYLATED; HESPERIDIN; HYPERGLYCEMIA; INSULIN RESISTANCE; LIVER; MALE; OXIDATION-REDUCTION; OXIDATIVE STRESS; OXIDOREDUCTASES; RATS; STREPTOZOCIN;

EID: 84868655005     PISSN: 10568727     EISSN: 1873460X     Source Type: Journal    
DOI: 10.1016/j.jdiacomp.2012.06.001     Document Type: Article

References (94)

1. A. Abdel-Moneim, M.B. Ashour, A.M. Mahmoud, and O.M. Ahmed Insulin sensitizing effects of hesperidin and naringin in experimental model of induced type 2 diabetes in rats: focus on tumor necrosis factor-alpha and resistin Nature and Science 7 10 2011 134 141
2. H. Aebi Catalase in vitro Methods in Enzymology 105 1984 121 126
3. O.M. Ahmed, A. Abdel-Moneim, I. Abulyazid, and A.M. Mahmoud Antihyperglycemic, antihyperlipidemic and antioxidant effects and the probable mechanisms of action of Ruta graveolens and rutin in nicotinamide/streptozotocin diabetic albino rats Diabetologia Croatica 39 1 2010 15 32
4. O.M. Ahmed, A.M. Mahmoud, A. Abdel-Moneim, and M.B. Ashour Antihyperglycemic and antihyperlipidemic effects of hesperidin and naringin in high fat diet/streptozotocin type 2 diabetic rats Life Science Journal 8 4 2011 91 101
5. American Diabetes Association Diagnosis and classification of diabetes mellitus Diabetes Care 30 Suppl. 1 2007 S42 S47
6. American Diabetic Association Consensus development conference on insulin resistance: 5-6 November 1997 Diabetes Care 21 1998 310 314
7. M. Aragno, R. Mastrocola, M.G. Catalano, E. Brignardello, O. Danni, and G. Boccuzzi Oxidative stress impairs skeletal muscle repair in diabetic rats Diabetes 53 2004 1082 1088
8. P. Arulselvan, and S.P. Subramanian Beneficial effects of Murraya koenigii leaves on antioxidant defense system and ultrastructural changes of pancreatic β-cells in experimental diabetes in rats Chemico-Biological Interactions 165 2007 155 164
9. H. Baker, O. Frank, B. Angelis, and S. Feingold Plasma tocopherol in man at various times after ingesting free or acetylated tocopherol Nutrition Reports International 21 1951 531 536
10. J.P. Bastard, M. Maachi, J. TranVan Nhieu, C. Jardel, E. Bruckert, and A. Grimaldi Adipose tissue IL-6 content correlates with resistance to insulin activation of glucose uptake both in vivo and in vitro Journal of Clinical Endocrinology and Metabolism 87 2002 2084 2089
11. J.P. Bastard, L. Pieroni, and B. Hainque Relationship between plasma plasminogen activator inhibitor 1 and insulin resistance Diabetes/Metabolism Research and Reviews 16 2000 192 201
12. E. Beutler, O. Duron, and B.M. Kelly Improved method for determination of blood glutathione Journal of Laboratory and Clinical Medicine 61 1963 882 888
13. A.D. Bolzán, and M.S. Bianchi Genotoxicity of streptozotocin Mutation Research 512 2002 121 134
14. Canadian Council on Animal Care Guide to the care and use of experimental animals vol. 2 1993 CCAC Ottawa, Ontario, Canada
15. M.K. Cha, and I.H. Kim Biochemical and Biophysical Research Communications 222 1996 619 625
16. H. Chen, M.H. Ward, and B.I. Graubard Dietary patterns and adenocarcinoma of the esophagus and distal stomach American Journal of Clinical Nutrition 75 2002 137 144
17. S.Y. Cho, J.Y. Park, E.M. Park, M.S. Choi, M.K. Lee, and S.M. Jeon Alternation of hepatic antioxidant enzyme activities and lipid profile in streptozotocin-induced diabetic rats by supplementation of dandelion water extract Clinica Chimica Acta 317 2002 109 117
18. S.C. Choe, H.S. Kim, T.S. Jeong, S.H. Bok, and T.B. Park Naringin as an anti atherogenic effect with the inhibition of intracellular adhesion molecule-1 in hypercholesterolemic rabbits Journal of Cardiovascular Pharmacology 38 2001 947 955
19. E.J. Choi Antioxidative effects of hesperetin against 7,12-dimethylbenz(a)anthracene-induced oxidative stress in mice Life Science 82 2008 1059 1064
20. E.J. Choi, and W.S. Ahn Neuroprotective effects of chronic hesperetin administration in mice Archives of Pharmacal Research 31 2008 1457 1462
21. L.F. Del Aguila, K.P. Claffey, and J.P. Kirwan TNF-alpha impairs insulin signaling and insulin stimulation of glucose uptake in C2C12 muscle cells American Journal of Physiology 276 1999 E849 E855
22. D. Dolphin, R. Poulson, and O. Avramovic Glutathione: Chemical, Biochemical and Metabolic Aspects, Vols. A and B 1989 J. Wiley and Sons New York, NY (pubs)
23. C. Gandhi, A. Upaganalawar, and R. Balaraman Protection against in vivo focal myocardial ischemia/reperfusion injury-induced arrhythmias and apoptosis by hesperidin Free Radical Research 2009 1 11
24. G. Gokce, and M.Z. Haznedaroglu Evaluation of antidiabetic, antioxidant and vasoprotective effects of Posidonia oceanica extract Journal of Ethnopharmacology 115 2008 122 130
25. D.E. Goldstein How much do you know about glycated hemoglobin testing Clinical Diabetes 13 1995 60 63
26. A. Green, S.B. Dobias, D.J. Walters, and A.R. Brasier Tumor necrosis factor increases the rate of lipolysis in primary cultures of adipocytes without altering levels of hormone-sensitive lipase Endocrinol. 134 1994 2581 2588
27. A.S. Greenberg, R.P. Nordan, J. McIntosh, J.C. Calvo, R.O. Scow, and D. Jablons Interleukin 6 reduces lipoprotein lipase activity in adipose tissue of mice in vivo and in 3T3-L1 adipocytes: a possible role for interleukin 6 in cancer cachexia Cancer Research 52 1992 4113 4116
28. S.M. Haffner, A.S. Greenberg, W.M. Weston, H. Chen, K. Williams, and M.I. Freed Effect of rosiglitazone treatment on nontraditional markers of cardiovascular disease in patients with type 2 diabetes mellitus Circulation 106 2002 679 684
29. B. Hasanain, and A.D. Mooradian Antioxidant vitamins and their influence in diabetes mellitus Current Diabetes Reports 2 2002 448 456
30. T. Hünkar, F. Aktan, A. Ceylan, and C. Karasu Antioxidants in Diabetes-Induced Complications (ADIC) Study Group. Effects of cod liver oil on tissue antioxidant pathways in normal and streptozotocin-diabetic rats Cell Biochemistry and Function 20 2002 297 302
31. S.K. Jain, K. Kannan, G. Lim, J. Matthew-Greer, R. McVie, and J.A. Bocchini Elevated blood interleukin-6 levels in hyperketonemic type 1 diabetic patients and secretion by acetoacetate-treated cultured U937 monocytes Diabetes Care 26 2003 2139 2143
32. S.K. Jain, K. Kannan, G. Lim, R. McVie, and J.A. Bocchini Hyperketonemia increases TNF-α secretion in cultured U937 monocytes and type-1 diabetic patients Diabetes 51 2002 2287 2293
33. S.E. Kahn, R.L. Hull, and K.M. Utzschneider Mechanisms linking obesity to insulin resistance and type 2 diabetes Nature 444 7121 2006 840 846
34. J. Kakadiya, M. Shah, and N.J. Shah Effect of nebivolol on serum diabetic marker and lipid profile in normal and streptozotocin-nicotinamide induced diabetic rats RJPBCS 1 2010 329 334
35. N. Kamalakannan, and P.S.M. Prince Antihyperglycaemic and antioxidant effect of rutin, a polyphenolic flavonoid, in streptozotocin-induced diabetic Wistar rats Basic & Clinical Pharmacology & Toxicology 98 2006 97 103
36. S. Kanno, A. Shouji, K. Asou, and M. Ishikawa Effects of naringin on hydrogen peroxide-induced cytotoxicity and apoptosis in P388 cells Journal of Pharmacological Sciences 92 2003 166 170
37. K. Karthikesan, L. Pari, and V.P. Menon Combined treatment of tetrahydrocurcumin and chlorogenic acid exerts potential antihyperglycemic effect on streptozotocin-nicotinamide-induced diabetic rats General Physiology and Biophysics 29 2010 23 30
38. A. Katsuki, Y. Sumida, S. Murashima, K. Murata, Y. Takarada, and K. Ito Serum levels of tumor necrosis factor-α are increased in obese patients with noninsulin-dependent diabetes mellitus Journal of Clinical Endocrinology and Metabolism 83 1998 859 862
39. P.A. Kern, S. Ranganathan, and C. Li Adipose tissue tumor necrosis factor and interleukin-6 expression in human obesity and insulin resistance American Journal of Physiology, Endocrinology and Metabolism 280 2001 E745 E751
40. 2 + influx Journal of Endocrinology 198 2008 549 560
41. J.Y. Kim, K.J. Jung, J.S. Choi, and H.Y. Chung Hesperetin: a potent antioxidant against peroxynitrite Free Radical Research 38 2004 761 769
42. D.H. Kim, E.A. Jung, I.S. Song, J.A. Han, T.H. Kim, and M.J. Han Intestinal bacterial metabolism of flavonoids and its relation to some biological activities Archives of Pharmacal Research 21 1998 17 23
43. G.P.S. Kumar, P. Arulselvan, D.S. Kumar, and S.P. Subramanian Anti-diabetic activity of fruits of Terminalia chebula on streptozotocin induced diabetic rats Journal of Health Science 52 3 2006 283 291
44. G. Kumar, G.S. Banu, and A.G. Murugesan Effect of Helicteres isora bark extracts on heart antioxidant status and lipid peroxidation in streptozotocin diabetic rats Journal of Applied Biomedicine 6 2008 89 95
45. P. Kumar, and A. Kumar Protective effect of hesperidin and naringin against 3-nitropropionic acid induced Huntington's like symptoms in rats: possible role of nitric oxide Behavioural Brain Research 206 2010 38 46
46. A. Kumar, and S.S. Sharma NF-κB inhibitory action of resveratrol: a probable mechanism of neuroprotection in experimental diabetic neuropathy Biochemical and Biophysical Research Communications 394 2010 360 365
47. E. Kume, H. Fujimura, N. Matsuki, M. Ito, C. Aruga, and W. Toriumi Hepatic changes in the acute phase of streptozotocin (SZ)-induced diabetes in mice Experimental and Toxicologic Pathology 55 2004 467 480
48. M. Laakso How good a marker is insulin level for insulin resistance? American Journal of Epidemiology 137 1993 959 965
49. C.H. Lang, C. Dobrescu, and G.J. Bagby Tumor necrosis factor impairs insulin action on peripheral glucose disposal and hepatic glucose output Endocrinol. 130 1992 43 52
50. P.R. Ling, C. Mueller, R.J. Smith, and B.R. Bistrian Hyperglycemia induced by glucose infusion causes hepatic oxidative stress and systemic inflammation, but not STAT3 or MAP kinase activation in liver in rats Metabolism 52 2003 868 874
51. R.R. Little, H.M. Wiedmeyer, J.D. England, A.L. Wilke, C.L. Rohlfing, and F.H. Wians Interlaboratory standardization of measurements of glycohemoglobins Clinical Chemistry 38 1992 2472 2478
52. Z. Liu, J. Li, Z. Zeng, M. Liu, and M. Wang The antidiabetic effects of cysteinyl metformin, a newly synthesized agent, in alloxan- and streptozocin-induced diabetic rats Chemico-Biological Interactions 173 2008 68 75
53. P. Manna, J. Das, J. Ghosh, and P.C. Sil Contribution of type 1 diabetes to rat liver dysfunction and cellular damage via activation of NOS, PARP, IκBα/NF-κB, MAPKs, and mitochondria-dependent pathways: prophylactic role of arjunolic acid Free Radical Biology & Medicine 48 2010 1465 1484
54. I. Maridonneau-Parini, P. Braquet, and R.P. Garay Heterogeneous effect of flavonoids on K + loss and lipid peroxidation induced by oxygen-free radicals in human red cells Pharmacological Research Communications 18 1986 61 72
55. A.C. Maritim, R.A. Sanders, and J.B. Watkins Diabetes, oxidative stress, and antioxidants: a review Journal of Biochemical and Molecular Toxicology 17 2003 2003 24 38
56. N. Marx, J. Froehlich, L. Siam, J. Ittner, G. Wierse, and A. Schmidt Antidiabetic PPARγ-activator rosiglitazone reduces MMP-9 serum levels in type 2 diabetic patients with coronary artery disease Arteriosclerosis, Thrombosis, and Vascular Biology 23 2003 283 288
57. R. MemiśǒgullarI, and E. Bakan Levels of ceruloplasmin, transferrin, and lipid peroxidation in the serum of patients with type 2 diabetes mellitus Journal of Diabetes and its Complications 18 2004 193 197
58. S. Muller, S. Martin, W. Koenig, P. Hanifi-Moghaddam, W. Rathmann, and B. Haastert Impaired glucose tolerance is associated with increased serum concentrations of interleukin 6 and co-regulated acute-phase proteins but not TNF-alpha or its receptors Diabetologia 45 2002 805 812
59. C. Nebot Spectrophotometric assay of superoxide dismutase activity based on the activated autoxidation of a tetracyclic catechol Analytical Biochemistry 214 1993 442 451
60. S.T. Omaye, T.D. Turnbull, and H.E. Sauberlich Selected method for the determination of ascorbic acid in animal cells, tissues and fluid D.B. McCormic, D.L. Wright, Methods in enzymology 1979 Academic press New York 3 11
61. E.C. Opara Oxidative stress, micronutrients, diabetes mellitus and its complications Journal of the Royal Society for the Promotion of Health 122 2002 28 34
62. S.J. Padayatty, A. Katz, Y. Wang, P. Eck, O. Kwon, and J.H. Lee Vitamin C as an antioxidant: evaluation of its role in disease prevention Journal of American College Health 22 2003 18 35
63. P. Palsamy, and S. Subramanian Ameliorative potential of resveratrol on proinflammatory cytokines, hyperglycemia mediated oxidative stress, and pancreatic cell dysfunction in streptozotocin-nicotinamide induced diabetic rats Journal of Cellular Physiology 224 2 2010 423 432
64. H. Parikh, E. Carlsson, W.A. Chutkow, L.E. Johansson, H. Storgaard, and P. Poulsen TXNIP regulates peripheral glucose metabolism in humans PLoS Medicine 4 5 2007 868 879
65. PC-STAT (1985). One way analysis of variance. Version IA (C). Program coded by Roa, M.; Blane, K. and Zonneberg, M. University of Georgia, USA.
66. J.C. Pickup Inflammation and activated innate immunity in the pathogenesis of type 2 diabetes Diabetes Care 27 2004 813 823
67. J.C. Pickup, G.C. Chusney, S.M. Thomas, and D. Burt Plasma interleukin-6, tumor necrosis factor alpha and blood cytokine production in types 2 diabetes Life Science 67 2000 291 300
68. K. Pradeep, S.H. Park, and K.C. Ko Hesperidin a flavanoglycone protects against gamma-irradiation induced hepatocellular damage and oxidative stress in Sprague-Dawley rats European Journal of Pharmacology 587 2008 273 280
69. R. Rahimi, S. Nikfar, B. Larijani, and M. Abdollahi A review on the role of antioxidants in the management of diabetes and its complications Biomedicine and Pharmacotherapy 59 2005 365 373
70. M. Rajadurai, and P.S. Prince Naringin ameliorates mitochondrial lipid peroxides, antioxidants and lipids in isoproterenol-induced myocardial infarction in Wistar rats Phytotherapy Research 23 2009 358 362
71. S. Ramachandran, K. Asokkumar, M. Uma Maheswari, T.K. Ravi, A.T. Sivashanmugam, and S. Saravanan Investigation of Antidiabetic, Antihyperlipidemic, and In vivo Antioxidant Properties of Sphaeranthus indicus Linn. in Type 1 Diabetic Rats: An Identification of Possible Biomarkers Evidence-Based Complementary and Alternative Medicine 2011 2011 1 8
72. S.V. Reddy, A.K. Tiwari, U.S. Kumar, R.J. Rao, and J.M. Rao Free radical scavenging, enzyme inhibitory constituents from antidiabetic Ayurvedic medicinal plant Hydnocarpus wightiana Blume Phytotherpy Research 19 2005 277 281
73. M.J. Reed, K. Meszaros, L.J. Entes, M.D. Claypool, J.G. Pinkett, and T.M. Gadbois A new rat model of type 2 diabetes, the fat-fed, streptozotocin- treated rat Metabolism 49 2000 1390 1394
74. P.M. Ridker, C.H. Hennekens, J.E. Buring, and N. Rifai C-reactive protein and other markers of inflammation in the prediction of cardiovascular disease in women New England Journal of Medicine 342 2000 836 843
75. T.R. Rosenstock, A.C. Carvalho, A. Jurkiewicz, R. Frussa-Filho, and S.S. Smaili Mitochondrial calcium, oxidative stress and apoptosis in a neurodegenerative disease model induced by 3-nitropropionic acid Journal of Neurochemistry 88 2004 1220 1228
76. V. Rotter, I. Nagaev, and U. Smith Interleukin-6 (IL-6) induces insulin resistance in 3T3-L1 adipocytes and is, like IL-8 and tumor necrosis factor-alpha, overexpressed in human fat cells from insulin-resistant subjects Journal of Biological Chemistry 278 2003 45777 45784
77. M. Ryden, A. Dicker, V. van Harmelen, H. Hauner, M. Brunnberg, and L. Perbeck Mapping of early signaling events in tumor necrosis factor-alpha- mediated lipolysis in human fat cells Journal of Biological Chemistry 277 2002 1085 1091
78. J.J. Senn, P.J. Klover, I.A. Nowak, and R.A. Mooney Interleukin-6 induces cellular insulin resistance in hepatocytes Diabetes 51 2002 3391 3399
79. G.C. Sheela, and K.T. Augusti antidiabetic effects of S-allyl cystine sulfoxide isolated from garlic Allium sativum Linn Indian Journal of Experimental Biology 30 1992 523 526
80. K. Shiratori, K. Ohgami, I. Ilieva, X.H. Jin, K. Yoshida, and S. Kase The effects of naringin and naringenin on endotoxin-induced uveitis in rats Journal of Ocular Pharmacology and Therapeutics 21 2005 298 304
81. K. Srinivasan, B. Viswanand, L. Asrat, C.L. Kaul, and P. Ramarao Combination of high-fat diet-fed and low dose of streptozotocin-treated rat: a model for type 2 diabetes and pharmacological screening Pharmacological Research 52 2005 313 320
82. K. Stadler, V. Jenei, G. von Bölcsházy, A. Somogyi, and J. Jakus Increased nitric oxide levels as an early sign of premature aging in diabetes Free Radical Biologie et Médecine 35 2003 1240 1251
83. R.H. Straub, H.W. Hense, and T. Andus Hormone replacement therapy and interrelation between serum interleukin-6 and body mass index in postmenopausal women: a population-based study Journal of Clinical Endocrinology and Metabolism 85 3 2000 1340 1344
84. T. Szkudelski The mechanism of alloxan and streptozotocin action of b-cells of the rat pancreas Physiological Research 50 2001 537 546
85. P. Trinder Determination of glucose in blood using glucose oxidase with an alternative oxygen acceptor Annals of Clinical Biochemistry 6 1969 24 27
86. M.J. Tunon, M.V. Garcia-Mediavilla, S. Sanchez-Campos, and J. Gonzalez-Gallego Potential of flavonoids as anti-inflammatory agents: modulation of proinflammatory gene expression and signal transduction pathways Current Drug Metabolism 10 2009 256 271
87. J. Turk, J.A. Corbett, S. Ramanadham, A. Bohrer, and M.L. McDaniel Biochemical evidence for nitric oxide formation from streptozotocin in isolated pancreatic islets Biochemical and Biophysical Research Communications 197 1993 1458 1464
88. C. West Radicals and oxidative stress in diabetes Diabetic Medicine 317 3 2000 171 180
89. S. Wild, G. Roglic, A. Green, R. Sicree, and H. King Global prevalence of diabetes: estimates for the year 2000 and projections for 2030 Diabetes Care 27 2004 1047 1053
90. World Health Organization (2006). Definition and diagnosis of diabetes mellitus and intermediate hyperglycemia: report of a WHO/IDF consultation. Geneva, Switzerland.
91. K. Yagi Lipid peroxides and human disease Chemistry and Physics of Lipids 45 1987 337 351
92. H. Yki-Jarvinen Drug Therapy: Thiazolidinediones New England Journal of Medicine 351 11 2004 1106 1118
93. S. Zhang, and K.H. Kim TNF-alpha inhibits glucose-induced insulin secretion in a pancreatic beta-cell line (INS-1) FEBS Letters 377 1995 237 239
94. W. Zhang, J. Zhao, J. Wang, X. Pang, X. Zhuang, and X. Zhu Hypo- glycemic effect of aqueous extract of sea buckthorn (Hippophae rhamnoides L.) seed residues in streptozotocin induced diabetic rats Phytotherpy Research 24 2010 228 232