Participation of antioxidant and cholinergic system in protective effect of naringenin against type-2 diabetes-induced memory dysfunction in rats

Neuroscience

Volumn 226, Issue , 2012, Pages 62-72

  Rahigude, A ^a   Bhutada, P ^a   Kaulaskar, S ^a   Aswar, M ^b   Otari, K ^c  

^a SINHGAD COLLEGE OF PHARMACY   (India)

^b Sinhgad Institute of Pharmacy   (India)

^c Rajgad Dyanpeeth's College of Pharmacy   (India)

Author keywords

Cholinesterase; Hippocampus; Memory; Novel object recognition; Pioglitazone; Type 2 diabetes

Indexed keywords

CHOLINESTERASE; DONEPEZIL; GLUCOSE; GLUTATHIONE; LIPID PEROXIDE; NARINGENIN; NITRIC OXIDE; PIOGLITAZONE; STREPTOZOCIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BODY WEIGHT; CHOLINERGIC SYSTEM; COGNITION; CONTROLLED STUDY; DRUG EFFECT; ENZYME ACTIVITY; ENZYME INHIBITION; GLUCOSE BLOOD LEVEL; HIPPOCAMPUS; LIPID DIET; MALE; MEMORY DISORDER; NEUROPROTECTION; NON INSULIN DEPENDENT DIABETES MELLITUS; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; RAT; RECOGNITION;

ANIMALS; ANTIOXIDANTS; BLOOD GLUCOSE; BODY WEIGHT; CHOLINESTERASE INHIBITORS; CHOLINESTERASES; DIABETES MELLITUS, EXPERIMENTAL; DIABETES MELLITUS, TYPE 2; DIETARY FATS; ESTROGEN ANTAGONISTS; FAT EMULSIONS, INTRAVENOUS; FLAVANONES; GLUTATHIONE; HYPOGLYCEMIC AGENTS; INDANS; LIPID PEROXIDATION; MALE; MEMORY DISORDERS; NITRIC OXIDE; PARASYMPATHETIC NERVOUS SYSTEM; PIPERIDINES; RATS; RATS, SPRAGUE-DAWLEY; RECOGNITION (PSYCHOLOGY); THIAZOLIDINEDIONES;

EID: 84867308972     PISSN: 03064522     EISSN: 18737544     Source Type: Journal    
DOI: 10.1016/j.neuroscience.2012.09.026     Document Type: Article

References (78)

1. Aigner T.G. Pharmacology of memory: cholinergic-glutamatergic interactions. Curr Opin Neurobiol 1995, 5:155-160.
2. Appleyard M.E. Non-cholinergic functions of acetylcholinesterase. Biochem Soc Trans 1994, 22:749-755.
3. Arvanitakis Z., Wilson R.S., Bienias J.L., Evans D.A., Bennett D.A. Diabetes mellitus and risk of Alzheimer disease and decline in cognitive function. Arch Neurol 2004, 61:661-666.
4. Baluchnejadmojarad T., Roghani M. Effect of naringenin on intracerebroventricular streptozotocin-induced cognitive deficits in rat: a behavioral analysis. Pharmacology 2006, 78:193-197.
5. Bhutada P., Mundhada Y., Bansod K., Bhutada C., Tawari S., Dixit P., Mundhada D. Ameliorative effect of quercetin on memory dysfunction in streptozotocin-induced diabetic rats. Neurobiol Learn Mem 2010, 94:293-302.
6. Bhutada P., Mundhada Y., Bansod K., Tawari S., Patil S., Dixit P., Umathe S., Mundhada D. Protection of cholinergic and antioxidant system contributes to the effect of berberine ameliorating memory dysfunction in rat model of streptozotocin-induced diabetes. Behav Brain Res 2011, 220:30-41.
7. Bhutada P., Mundhada Y., Humane V., Rahigude A., Deshmukh P., Latad S., Jain K. Agmatine, an endogenous ligand of imidazoline receptor protects against memory impairment and biochemical alterations in streptozotocin-induced diabetic rats. Prog Neuropsychopharmacol Biol Psychiatry 2012, 37:96-105.
8. Biessels G.J., Kamal A., Ramakers G.M., Urban I.U., Spruijt D., Erkelens D.W., Gispen W.H. Place learning and hippocampal synaptic plasticity in streptozotocin-induced diabetic rats. Diabetes 1996, 45:1259-1266.
9. Biessels G.J., Heide L.P., Kamal A. Ageing and diabetes: implications for brain function. Eur J Pharmacol 2002, 441:1-14.
10. Biessels G.J., De Leeuw F.E., Lindeboom J., Barkhof F., Scheltens P. Increased cortical atrophy in patients with Alzheimer's disease and type 2 diabetes mellitus. J Neurol Neurosurg Psychiatry 2006, 77:304-307.
11. Biessels G.J., Kerssen A., de Haan E.H., Kappelle L.J. Cognitive dysfunction and diabetes: implications for primary care. Prim Care Diabetes 2007, 1:187-193.
12. Borradaile N.M., de Dreu L.E., Barrett P.H., Huff M.W. Inhibition of hepatocyte apoB secretion by naringenin: enhanced rapid intracellular degradation independent of reduced microsomal cholesteryl esters. J Lipid Res 2002, 43:1544-1554.
13. Borradaile N.M., de Dreu L.E., Barrett P.H., Behrsin C.D., Huff M.W. Hepatocyte apoB-containing lipoprotein secretion is decreased by the grapefruit flavonoid, naringenin, via inhibition of MTP-mediated microsomal triglyceride accumulation. Biochemistry 2003, 42:1283-1291.
14. Cao Q., Jiang K., Zhang M., Liu Y., Xiao S., Zuo C., Huang H. Brain glucose metabolism and neuropsychological test in patients with mild cognitive impairment. Chin Med J (Engl) 2003, 116:1235-1238.
15. Cardoso S., Santos M.S., Seiça R., Moreira P.I. Cortical and hippocampal mitochondria bioenergetics and oxidative status during hyperglycemia and/or insulin-induced hypoglycemia. Biochim Biophys Acta 2010, 1802:942-951.
16. Chui M.H., Greenwood C.E. Antioxidant vitamins reduce acute meal-induced memory deficits in adults with type-2 diabetes. Nutr Res 2008, 28:423-429.
17. Cosway R., Strachan M.W., Dougall A., Frier B.M., Deary I.J. Cognitive function and information processing in type 2 diabetes. Diabet Med 2001, 18:803-810.
18. de la Tremblaye P.B., Plamondon H. Impaired conditioned emotional response and object recognition are concomitant to neuronal damage in the amygdala and perirhinal cortex in middle-aged ischemic rats. Behave. Brain Res 2011, 219:227-233.
19. Eichenbaum H., Schoenbaum G., Young B., Bunsey M. Functional organization of the hippocampal memory system. Proc Natl Acad Sci U S A 1996, 93:13500-13507.
20. Ellman G.L. Tissue sulfhydryl groups. Arch Biochem Biophy 1959, 82:70-77.
21. Ellman G.L., Courtney K.D., Abdres V., Feather-stone R.M. A new rapid colorimetric determination of acetylcholinesterase activity. Biochem Pharmacol 1961, 88-95.
22. Farr S.A., Banks W.A., Uezu K., Gaskin F.S., Morley J.E. DHEAS improves learning and memory in aged SAMP8 mice but not in diabetic mice. Life Sci 2004, 75:2775-2785.
23. Fukui K., Onodera K., Shinkai T., Suzuki S., Urano S. Impairment of learning and memory in rats caused by oxidative stress and aging, and changes in antioxidative defense systems. Ann N Y Acad Sci 2001, 928:168-175.
24. Gallagher M., Colombo P.J. Ageing: the cholinergic hypothesis of cognitive decline. Curr Opin Neurobiol 1995, 5:161-168.
25. Gispen W.H., Biessels G.J. Cognition and synaptic plasticity in diabetes mellitus. Trends Neurosci 2000, 23:542-549.
26. Goldwasser J., Cohen P.Y., Yang E., Balaguer P., Yarmush M.L., Nahmias Y. Transcriptional regulation of human and rat hepatic lipid metabolism by the grapefruit flavonoid naringenin: role of PPARalpha, PPARgamma and LXRalpha. PLoS One 2010, 5:e12399.
27. Green L., Wagner D., Glogowski J., Skipper P., Wishnok J. Analysis of nitrate, nitrite, and [15N] nitrate in biological fluids. Anal Biochem 1982, 126:131-138.
28. Greenwood C.E., Winocur G. Learning and memory impairment in rats fed a high saturated fat diet. Behav Neural Biol 1990, 53:74-87.
29. Guelzim N., Huneau J.F., Mathé V., Quignard-Boulangé A., Martin P.G., Tomé D., Hermier D. Consequences of PPAR(α) invalidation on glutathione synthesis: interactions with dietary fatty acids. PPAR Res 2011, 2011:256186.
30. Hasanein P., Shahidi S. Effects of combined treatment with vitamins C and E on passive avoidance learning and memory in diabetic rats. Neurobiol Learn Mem 2010, 93:472-480.
31. Hasselmo M.E., Sarter M. Modes and models of forebrain cholinergic neuromodulation of cognition. Neuropsychopharmacology 2011, 36:52-73.
32. Heitner J., Dickson D. Diabetics do not have increased Alzheimer-type pathology compared with age-matched control subjects. A retrospective postmortem immunocytochemical and histofluorescent study. Neurology 1997, 49:1306-1311.
33. Heo H.J., Kim D.O., Shin S.C., Kim M.J., Kim B.G., Shin D.H. Effect of antioxidant flavanone, naringenin, from Citrus junos on neuroprotection. J Agric Food Chem 2004, 52:1520-1525.
34. Heo H.J., Kim M.J., Lee J.M., Choi S.J., Cho H.Y., Hong B., Kim H.K., Kim E., Shin D.H. Naringenin from Citrus junos has an inhibitory effect on acetylcholinesterase and a mitigating effect on amnesia. Dement Geriatr Cogn Disord 2004, 17:151-157.
35. Horiba T., Nishimura I., Nakai Y., Abe K., Sato R. Naringenin chalcone improves adipocyte functions by enhancing adiponectin production. Mol Cell Endocrinol 2010, 323:208-214.
36. Jiang L.Y., Tang S.S., Wang X.Y., Liu L.P., Long Y., Hu M., Liao M.X., Ding Q.L., Hu W., Li J.C., Hong H. PPARγ agonist pioglitazone reverses memory impairment and biochemical changes in a mouse model of type 2 diabetes mellitus. CNS Neurosci Ther 2012, 18:659-666.
37. Kamal A., Biessels G.J., Gispen W.H., Ramakers G.M. Synaptic transmission changes in the pyramidal cells of the hippocampus in streptozotocin-induced diabetes mellitus in rats. Brain Res 2006, 1074:276-280.
38. Kannappan S., Palanisamy N., Anuradha C.V. Suppression of hepatic oxidative events and regulation of eNOS expression in the liver by naringenin in fructose-administered rats. Eur J Pharmacol 2010, 645:177-184.
39. Kanoski S.E., Meisel R.L., Mullins A.J., Davidson T.L. The effects of energy-rich diets on discrimination reversal learning and on BDNF in the hippocampus and prefrontal cortex of the rat. Behav Brain Res 2007, 182:57-66.
40. Kim H.B., Jang M.H., Shin M., Lim B.V., Kim Y.P., Kim K.J. Treadmill exercise increase cell proliferation in dentate gyrus of rats with streptozotocin-induced diabetes. J Diabetes Complications 2003, 17:23-29.
41. Kuhad A., Sethi R., Chopra K. Lycopene attenuates diabetes-associated cognitive decline in rats. Life Sci 2008, 83:128-134.
42. Lu J., Wu D.M., Zheng Y.L., Hu B., Cheng W., Zhang Z.F., Shan Q. Ursolic acid improves high fat diet-induced cognitive impairments by blocking endoplasmic reticulum stress and IκB kinase β/nuclear factor-κB-mediated inflammatory pathways in mice. Brain Behav Immun 2011, 25(8):1658-1667.
43. Luchsinger J.A., Tang M.X., Shea S., Mayeux R. Caloric intake and the risk of Alzheimer disease. Arch Neurol 2002, 59:1258-1263.
44. Mesulam M.M., Hersh L.B., Mash D.C., Geula C. Differential cholinergic innervation within functional subdivisions of the human cerebral cortex: a choline acetyltransferase study. J Comp Neurol 1992, 318:316-328.
45. Molteni R., Ying Z., Gómez-Pinilla F. Differential effects of acute and chronic exercise on plasticity-related genes in the rat hippocampus revealed by microarray. Eur J Neurosci 2002, 16:1107-1116.
46. Moskaug J.Ø., Carlsen H., Myhrstad M.C., Blomhoff R. Polyphenols and glutathione synthesis regulation. Am J Clin Nutr 2005, 81:277S-283S.
47. Mulvihill E.E., Allister E.M., Sutherland B.G., Telford D.E., Sawyez C.G., Edwards J.Y., Markle J.M., Hegele R.A., Huff M.W. Naringenin prevents dyslipidemia, apolipoprotein B overproduction, and hyperinsulinemia in LDL receptor-null mice with diet-induced insulin resistance. Diabetes 2009, 58:2198-2210.
48. Nishikawa T., Edelstein D., Du X.L., Yamagishi S., Matsumura T., Kaneda Y. Normalizing mitochondrial superoxide production blocks three pathways of hyperglycaemic damage. Nature 2000, 404:787-790.
49. Northam E.A., Rankins D., Lin A., Wellard R.M., Pell G.S., Finch S.J. Central nervous system functions in youth with type 1 diabetes 12years after disease onset. Diabetes Care 2009, 32:445-450.
50. Ohkawa H., Ohishi N., Yagi K. Assay for lipid peroxides in animal tissues by thiobarbituric acid reaction. Anal Biochem 1979, 95:351-358.
51. Olsen H.T., Stafford G.I., van Staden J., Christensen S.B., Jäger A.K. Isolation of the MAO inhibitor naringenin from menthaaquatica L. J Ethnopharmacol 2008, 117:500-502.
52. Oršolić N., Gajski G., Garaj-Vrhovac V., Dikić D., Prskalo Z.Š., Sirovina D. DNA-protective effects of quercetin or naringenin in alloxan-induced diabetic mice. Eur J Pharmacol 2011, 656:110-118.
53. Ortiz-Andrade R.R., Sánchez-Salgado J.C., Navarrete-Vázquez G., Webster S.P., Binnie M., García-Jiménez S., León-Rivera I., Cigarroa-Vázquez P., Villalobos-Molina R., Estrada-Soto S. Antidiabetic and toxicological evaluations of naringenin in normoglycaemic and NIDDM rat models and its implications on extra-pancreatic glucose regulation. Diabetes Obes Metab 2008, 10:1097-1104.
54. Parikh V., Kozak R., Martinez V., Sarter M. Prefrontal acetylcholine release controls cue detection on multiple timescales. The first study that employed enzyme-coated microelectrodes to monitor real-time acetylcholine release in performing animals and concluded that cholinergic transients mediated cue detection. Neuron 2007, 56:141-154.
55. Park J.-H., Lee J.-W., Paik H.-D., Cho S.G., Nah S.-Y., Park Y.-S., Han Y.S. Cytotoxic effects of 7-O-butyl naringenin on human breast cancer MCF-7 cells. Food Sci Biotechnol 2010, 19:717-724.
56. Park H.R., Park M., Choi J., Park K.Y., Chung H.Y., Lee J. A high-fat diet impairs neurogenesis: involvement of lipid peroxidation and brain-derived neurotrophic factor. Neurosci Lett 2010, 482:235-239.
57. Pascalis O., Hunkin N.M., Bachevalier J., Mayes A.R. Change in background con- text disrupts performance on visual paired comparison following hippocampal damage. Neuropsychologia 2009, 47:2107-2113.
58. Pasquier F., Boulogne A., Leys D., Fontaine P. Diabetes mellitus and dementia. Diabetes Metab 2006, 32:403-414.
59. Piazza F.V., Pinto G.V., Trott G., Marcuzzo S., Gomez R., Fernandes M.C. Enriched environment prevents memory deficits in type 1 diabetic rats. Behav Brain Res 2011, 217:16-20.
60. Pipatpiboon N., Pratchayasakul W., Chattipakorn N., Chattipakorn S.C. PPARγ agonist improves neuronal insulin receptor function in hippocampus and brain mitochondria function in rats with insulin resistance induced by long term high-fat diets. Endocrinology 2012, 153:329-338.
61. Rayidi S. Effect of naringenin on carbohydrate metabolism in STZ-nicotinamide induced diabetic rats. Biomirror 2011, 2:1-9.
62. Revsin Y., Rekers N.V., Louwe M.C., Saravia F.E., De Nicola A.F., de Kloet E.R. Glucocorticoid receptor blockade normalizes hippocampal alterations and cognitive impairment in streptozotocin-induced type 1 diabetes mice. Neuropsychopharmacology 2009, 34:747-758.
63. Ribeiro I.A., Rocha J., Sepodes B., Mota-Filipe Y., Ribeiro M.H. Effect of naringin enzymatic hydrolysis towards naringenin on the anti-inflammatory activity of both compounds. J Mol Catal B Enzym 2008, 52:13-18.
64. Ryan C.M., Freed M.I., Rood J.A., Cobitz A.R., Waterhouse B.R., Strachan M.W. Improving metabolic control leads to better working memory in adults with type 2 diabetes. Diabetes Care 2006, 29:345-351.
65. Sanchez-Chavez G., Salceda R. Effect of streptozotocin-induced diabetes on activities of cholinesterases in the rat retina. IUBMB Life 2000, 49:283-287.
66. Schmatz R., Mazzanti C.M., Spanevello R., Stefanello N., Gutierres J., Correa M., da Rosa M.M., Rubin M.A., Chitolina Schetinger M.R., Morsch V.M. Resveratrol prevents memory deficits and the increase in acetylcholinesterase activity in streptozotocin-induced diabetic rats. Eur J Pharmacol 2009, 610:42-48.
67. Sima A.A., Kamiya H., Li Z.G. Insulin, C-peptide, hyperglycemia, and central nervous system complications in diabetes. Eur J Pharmacol 2004, 490:187-197.
68. Srinivasan K., Viswanad B., Asrat L., Kaul C.L., Ramarao P. Combination of high-fat diet-fed and low-dose streptozotocin-treated rat: a model for type 2 diabetes and pharmacological screening. Pharmacol Res 2005, 52:313-320.
69. Steen E., Terry B.M., Rivera E.J., Cannon J.L., Neely T.R., Tavares R., Xu X.J., Wands J.R., de la Monte S.M. Impaired insulin and insulin-like growth factor expression and signaling mechanisms in Alzheimer's disease - is this type 3 diabetes?. J Alzheimers Dis 2005, 7:63-80.
70. Tuzcu M., Baydas G. Effect of melatonin and vitamin E on diabetes-induced learning and memory impairment in rats. Eur J Pharmacol 2006, 537:106-110.
71. Wilcox L.J., Borradaile N.M., Huff M.W. Antiatherogenic properties of naringenin, a citrus flavonoid. Cardiovasc Drug Rev 1999, 17:160-178.
72. Winocur G., Greenwood C.E. The effects of high fat diets and environmental influences on cognitive performance in rats. Behav Brain Res 1999, 101:153-161.
73. Wu J.H., Haan M.N., Liang J., Ghosh D., Gonzalez H.M., Herman W.H. Impact of diabetes on cognitive function among older Latinos: a population-based cohort study. J Clin Epidemiol 2003, 56:686-693.
74. Xu D., Xu M., Lin L., Rao S., Wang J., Davey A.K. The effect of isosteviol on hyperglycemia and dyslipidemia induced by lipotoxicity in rats fed with high-fat emulsion. Life Sci 2012, 90:30-38.
75. Zbarsky V., Datla K.P., Parkar S., Rai D.K., Aruoma O.I., Dexter D.T. Neuroprotective properties of the natural phenolic antioxidants curcumin and naringenin but not quercetin and fisetin in a 6-OHDA model of Parkinson's disease. Free Radic Res 2005, 39:1119-1125.
76. Zhang T., Pan B.S., Sun G.C., Sun X., Sun F.Y. Diabetes synergistically exacerbates poststroke dementia and tau abnormality in brain. Neurochem Int 2010, 56:955-961.
77. Zhao W.Q., Chen H., Quon M.J., Alkon D.L. Insulin and the insulin receptor in experimental models of learning and memory. Eur J Pharmacol 2004, 490:71-78.
78. Zhao W.Q., Townsend M. Insulin resistance and amyloidogenesis as common molecular foundation for type 2 diabetes and Alzheimer's disease. Biochim Biophys Acta 2009, 1792:482-496.