277
Views
33
CrossRef citations to date
0
Altmetric
Original Article

Ameliorative effect of naringenin on hyperglycemia-mediated inflammation in hepatic and pancreatic tissues of Wistar rats with streptozotocin- nicotinamide-induced experimental diabetes mellitus

, &
Pages 793-803 | Received 20 Apr 2013, Accepted 05 Jul 2013, Published online: 08 Aug 2013

References

  • Brunner Y, Schvartz D, Priego-Capote F, Coute Y, Sanchez JC. Glucotoxicity and pancreatic proteomics. J Proteomics 2009;71:576–591.
  • Poitout V, Amyot J, Semache M, Zarrouki B, Hagman D, Fontés G. Glucolipotoxicity of the pancreatic beta cell. Biochim Biophys Acta 2010;1801:289–298.
  • Haluzik M, Nedvidkova J. The role of nitric oxide in the development of streptozotocin-induced diabetes mellitus: experimental and clinical implications. Physiol Res 2000;49: S37–S42.
  • King GL, Loeken MR. Hyperglycemia-induced oxidative stress in diabetic complications. Histochem Cell Biol 2004;122:333–338.
  • Brownlee M. A radical explanation for glucose-induced beta cell dysfunction. J Clin Invest 2003;112:1788–1790.
  • Scott JA, King GL. Oxidative stress and antioxidant treatment in diabetes. Ann N Y Acad Sci 2004;1031:204–213.
  • Evans JL, Goldfine ID, Maddux BA, Grodsky GM. Oxidative stress and stress-activated signaling pathways: a unifying hypothesis of type 2 diabetes. Endocr Rev 2002;23: 599–622.
  • Gabay C, Kushner I. Acute-phase proteins and other systemic responses to inflammation. N Engl J Med 1999;340: 448–454.
  • Baker RG, Hayden MS, Ghosh S. NF-kappaB, inflammation, and metabolic disease. Cell Metab 2011;13:11–22.
  • Nunokawa Y, Oikawa S, Tanaka S. Human inducible nitric oxide synthase gene is transcriptionally regulated by nuclear factor-kappaB dependent mechanism. Biochem Biophys Res Commun 1996;223:347–352.
  • Tanaka Y, Shimizu H, Sato N, Mori M, Shimomura Y. Involvement of spontaneous nitric oxide production in the diabetogenic action of streptozotocin. Pharmacology 1995; 50:69–73.
  • Tak PP, Firestein GS. NF-kappaB: a key role in inflammatory diseases. J Clin Invest 2001;107:7–11.
  • Annadurai T, Muralidharan AR, Joseph T, Hsu MJ, Thomas PA, Geraldine P. Antihyperglycemic and antioxidant effects of a flavanone, naringenin, in streptozotocin–nicotinamide-induced experimental diabetic rats. J Physiol Biochem 2012;68:307–318.
  • Raza SS, Khan MM, Ahmad A, Ashafaq M, Islam F, Wagner AP, et al. Neuroprotective effect of naringenin is mediated through suppression of NF-κB signaling pathway in experimental stroke. Neuroscience 2013;230:157–171.
  • Yang J, Li Q, Zhou XD, Kolosov VP, Perelman JM. Naringenin attenuates mucous hypersecretion by modulating reactive oxygen species production and inhibiting NF-κB activity via EGFR-PI3K-Akt/ERK MAPKinase signaling in human airway epithelial cells. Mol Cell Biochem 2011;351: 29–40.
  • Rakieten N, Rakieten ML, Nadkarni MR. Studies on the diabetogenic action of streptozotocin (NSC-37917). Cancer Chemother Rep 1963;29:91–98.
  • 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;47:224–229.
  • Bradford M. A rapid and sensitive method for the quantification of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 1976;72:248–254.
  • Sambrook. J, Fritsch EF, Maniatis T. 1989. Molecular cloning: a laboratory manual. 2nd ed. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press.
  • Green LC, Wagner DA, Glogowski J, Skipper PL, Wishnok JS, Tannenbaum SR. Analysis of nitrate, nitrite, and [15N]nitrate in biological fluids. Anal Biochem 1982;126:131–138.
  • Kajimoto Y, Kaneto H. Role of oxidative stress in pancreatic beta-cell dysfunction. Ann N Y Acad Sci 2004;1011:168–176.
  • LeDoux SP, Hall CR, Forbes PM, Patton NJ, Wilson GL. Mechanisms of nicotinamide and thymidine protection from alloxan and streptozocin toxicity. Diabetes 1988;37: 1015–1019.
  • Birt DF, Hendrich S, Wang W. Dietary agents in cancer prevention: flavonoids and isoflavonoids. Pharmacol Ther 2001;90:157–177.
  • Hamalainen M, Nieminen R, Vuorela P, Heinonen M, Moilanen E. Anti-inflammatory effects of flavonoids: genistein, kaempferol, quercetin, and daidzein inhibit STAT-1 and NF-kappaB activations, whereas flavone, isorhamnetin, naringenin, and pelargonidin inhibit only NF-kappaB activation along with their inhibitory effect on iNOS expression and NO production in activated macrophages. Mediators Inflamm 2007;2007:45673.
  • Vafeiadou K, Vauzour D, Lee HY, Rodriguez-Mateos A, Williams RJ, Spencer JP. The citrus flavanone naringenin inhibits inflammatory signalling in glial cells and protects against neuroinflammatory injury. Arch Biochem Biophys 2009;484:100–109.
  • El Mohsen MA, Marks J, Kuhnle G, Rice-Evans C, Moore K, Gibson G, et al. The differential tissue distribution of the citrus flavanone naringenin following gastric instillation. Free Radic Res 2004;38:1329–1340.
  • Erlund I, Meririnne E, Alfthan G, Aro A. Plasma kinetics and urinary excretion of the flavanones naringenin and hesperetin in humans after ingestion of orange juice and grapefruit juice. J Nutr 2001;131:235–241.
  • Navarro JF, Mora C, Maca M, Garca J. Inflammatory parameters are independently associated with urinary albumin in type 2 diabetes mellitus. Am J Kidney Dis 2003;42:53–61.
  • Andresdottir MB, Sigfusson N, Sigvaldason H, Gudnason V. Erythrocyte sedimentation rate, an independent predictor of coronary heart disease in men and women: The Reykjavik Study. Am J Epidemiol 2003;158:844–851.
  • Maiti R, Agrawal NK, Dash D, Pandey BL. Effect of Pentoxifylline on inflammatory burden, oxidative stress and platelet aggregability in hypertensive type 2 diabetes mellitus patients. Vascul Pharmacol 2007;47:118–124.
  • Pepys MB, Hirschfield GM. C-reactive protein: a critical update. J Clin Invest 2003;111:1805–1812.
  • Ridker PM, Buring JE, Shih J, Matias M, Hennekens CH. Prospective study of C-reactive protein and the risk of future cardiovascular events among apparently healthy women. Circulation 1998;98:731–733.
  • D’Alessandris C, Lauro R, Presta I, Sesti G. C-reactive protein induces phosphorylation of insulin receptor substrate-1 on Ser307 and Ser 612 in L6 myocytes, thereby impairing the insulin signalling pathway that promotes glucose transport. Diabetologia 2007;50:840–849.
  • Feldmann M, Brennan FM, Maini R. Cytokines in autoimmune disorders. Int Rev Immunol 1998;17:217–228.
  • Mannel DN, Echtenacher B. TNF in the inflammatory response. Chem Immunol 2000;74:141–161.
  • Crook M. Type 2 diabetes mellitus: a disease of the innate immune system?An update. Diabet Med 2004;21: 203–207.
  • Oakley F, Mann J, Nailard S, Smart DE, Mungalsingh N, Constandinou C, et al. Nuclear factor-kappaB1 (p50) limits the inflammatory and fibrogenic responses to chronic injury. Am J Pathol 2005;166:695–708.
  • Shoelson SE, Lee J, Goldfine AB. Inflammation and insulin resistance. J Clin Invest 2006;116:1793–1801.
  • Simpson KJ, Lukacs NW, Colletti L, Strieter RM, Kunkel SL. Cytokines and the liver. J Hepatol 1997;27:1120–1132.
  • Palsamy P, Subramanian S. Ameliorative potential of resveratrol on proinflammatory cytokines, hyperglycemia mediated oxidative stress, and pancreatic beta-cell dysfunction in streptozotocin-nicotinamide-induced diabetic rats. J Cell Physiol 2010;224:423–432.
  • Barnes PJ, Karin M. Nuclear factor-kappaB: a pivotal transcription factor in chronic inflammatory diseases. N Engl J Med 1997;336:1066–1071.
  • Singh R, Barden A, Mori T, Beilin L. Advanced glycation end-products: a review. Diabetologia 2001;44:129–146.
  • Okazaki T, Sakon S, Sasazuki T, Sakurai H, Doi T, Yagita H, et al. Phosphorylation of serine 276 is essential for p65 NF-kappaB subunit-dependent cellular responses. Biochem Biophys Res Commun 2003;300:807–812.
  • Vermeulen L, De Wilde G, Van Damme P, Vanden Berghe W, Haegeman G. Transcriptional activation of the NF-kappaB p65 subunit by mitogen- and stress-activated protein kinase-1 (MSK1). EMBO J 2003;22:1313–1324.
  • Chen F. Is NF-kappaB a culprit in type 2 diabetes?Biochem Biophys Res Commun 2005;332:1–3.
  • Mariappan N, Elks CM, Sriramula S, Guggilam A, Liu Z, Borkhsenious O, Francis J. NF-κB-induced oxidative stress contributes to mitochondrial and cardiac dysfunction in type II diabetes. Cardiovasc Res 2010;85:473–483.
  • Dias AS, Porawski M, Alonso M, Marroni N, Collado PS, Gonzalez-Gallego J. Quercetin decreases oxidative stress, NF-kappaB activation, and iNOS overexpression in liver of streptozotocin-induced diabetic rats. J Nutr 2005;135: 2299–2304.
  • Sivakumar S, Palsamy P, Subramanian SP. Attenuation of oxidative stress and alteration of hepatic tissue ultrastructure by D-pinitol in streptozotocin-induced diabetic rats. Free Radic Res 2010;44:668–678.
  • Kroncke KD, Fehsel K, Kolb-Bachofen V. Inducible nitric oxide synthase in human diseases. Clin Exp Immunol 1998;113:147–156.
  • Rosa SC, Judas F, Lopes MC, Mendes AF. Nitric oxide synthase isoforms and NF-kappaB activity in normal and osteoarthritic human chondrocytes: regulation by inducible nitric oxide. Nitric Oxide 2008;19:276–283.
  • Kim EK, Kwon KB, Koo BS, Han MJ, Song MY, Song EK, et al. Activation of peroxisome proliferator-activated receptor-gamma protects pancreatic beta-cells from cytokine-induced cytotoxicity via NF kappaB pathway. Int J Biochem Cell Biol 2007;39:1260–1275.
  • Kaneto H, Fujii J, Seo HG, Suzuki K, Matsuoka T, Nakamura M, et al. Apoptotic cell death triggered by nitric oxide in pancreatic beta-cells. Diabetes 1995;44:733–738.
  • Stadler K, Jenei V, von Bolcshazy G, Somogyi A, Jakus J. Role of free radicals and reactive nitrogen species in the late complications of diabetes mellitus in rats. Orv Hetil 2004; 145:1135–1140.

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.