Naringin ameliorates memory deficits in experimental paradigm of Alzheimer's disease by attenuating mitochondrial dysfunction

Pharmacology Biochemistry and Behavior

Volumn 127, Issue , 2014, Pages 101-110

  Sachdeva, Anand Kamal ^a   Kuhad, Anurag ^a   Chopra, Kanwaljit ^a  

^a PANJAB UNIVERSITY   (India)

Author keywords

Cognitive impairment; ICV STZ; IL 1 ; Mitochondrial dysfunction; Naringin; TNF

Indexed keywords

ACETYLCHOLINESTERASE; AURANTIIN; CATALASE; INTERLEUKIN 1BETA; MITOCHONDRIAL ENZYME; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE DEHYDROGENASE; RIVASTIGMINE; STREPTOZOCIN; SUCCINATE DEHYDROGENASE; SUPEROXIDE DISMUTASE; TUMOR NECROSIS FACTOR ALPHA; FLAVANONES; NARINGIN;

ALZHEIMER DISEASE; AMNESIA; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BRAIN CORTEX; BRAIN LEVEL; COGNITIVE DEFECT; CONTROLLED STUDY; CYTOKINE RELEASE; DISORDERS OF MITOCHONDRIAL FUNCTIONS; DOSE RESPONSE; DRUG EFFECT; ELEVATED PLUS MAZE TEST; ENZYME ACTIVITY; HIPPOCAMPUS; LONG TERM CARE; MALE; MORRIS WATER MAZE TEST; NITROSATIVE STRESS; NONHUMAN; OXIDATIVE STRESS; RAT; TASK PERFORMANCE; ANIMALS; DOSE-RESPONSE RELATIONSHIP, DRUG; DRUG EFFECTS; MEMORY DISORDERS; METABOLISM; MITOCHONDRIA; PHYSIOLOGY; PSYCHOLOGY; RANDOM ALLOCATION; RATS; RATS, WISTAR;

ALZHEIMER DISEASE; ANIMALS; DOSE-RESPONSE RELATIONSHIP, DRUG; FLAVANONES; MALE; MEMORY DISORDERS; MITOCHONDRIA; RANDOM ALLOCATION; RATS; RATS, WISTAR;

EID: 84910608223     PISSN: 00913057     EISSN: 18735177     Source Type: Journal    
DOI: 10.1016/j.pbb.2014.11.002     Document Type: Article

References (64)

1. A. Aggarwal, V. Gaur, and A. Kumar Nitric oxide mechanism in the protective effect of naringin against post-stroke depression (PSD) in mice Life Sci 86 2010 928 935
2. T. Baluchnejadmojarad, and M. Roghani Effect of naringenin on intracerebroventricular streptozotocin-induced cognitive deficits in rat: a behavioral analysis Pharmacology 78 2006 193 197
3. S.B. Berman, and T.G. Hastings Dopamine oxidation alters mitochondrial respiration and induces permeability transition in brain mitochondria J Neurochem 73 1999 1127 1137
4. A. Blokland, and J. Jolles Spatial learning deficit and reduced hippocampal ChAT activity in rats after an ICV injection of streptozotocin Pharmacol Biochem Behav 44 1993 491 494
5. P.-E. Chabrier, C. Demerle-Pallardy, and M. Auguet Nitric oxide synthases: targets for therapeutic strategies in neurological diseases Cell Mol Life Sci 55 1999 1029 1035
6. C. Chen, S. Lang, P. Zuo, N. Yang, X. Wang, and C. Xia Effects of D-galactose on the expression of hippocampal peripheral-type benzodiazepine receptor and spatial memory performances in rats Psychoneuroendocrinology 31 2006 805 811
7. S.-C. Choe, H.-S. Kim, T.-S. Jeong, S.-H. Bok, and Y.-B. Park Naringin has an antiatherogenic effect with the inhibition of intercellular adhesion molecule-1 in hypercholesterolemic rabbits J Cardiovasc Pharmacol 38 2001 947 955
8. A. Claiborne Catalase activity CRC handbook of methods for oxygen radical research 1 1985 283 284
9. E. Clementi, G.C. Brown, M. Feelisch, and S. Moncada Persistent inhibition of cell respiration by nitric oxide: crucial role of S-nitrosylation of mitochondrial complex I and protective action of glutathione Proc Natl Acad Sci U S A 95 1998 7631
10. D. Cumiskey, M. Butler, P. Moynagh, and J. O'connor Evidence for a role for the group I metabotropic glutamate receptor in the inhibitory effect of tumor necrosis factor-α on long-term potentiation Brain Res 1136 2007 13 19
11. A. Dhir, and S.K. Kulkarni Venlafaxine reverses chronic fatigue-induced behavioral, biochemical and neurochemical alterations in mice Pharmacol Biochem Behav 89 2008 563 571
12. A. Eckert, U. Keil, C.A. Marques, A. Bonert, C. Frey, and K. Schüssel Mitochondrial dysfunction, apoptotic cell death, and Alzheimer's disease Biochem Pharmacol 66 2003 1627 1634
13. G.L. Ellman, K.D. Courtney, and R.M. Featherstone A new and rapid colorimetric determination of acetylcholinesterase activity Biochem Pharmacol 7 1961 88 95
14. U. Fuhr, and A.L. Kummert The fate of naringin in humans: A key to grapefruit juice-drug interactions? Clin Pharmacol Ther 58 1995 365 373
15. M. Ganguli, V. Chandra, M.I. Kamboh, J.M. Johnston, H.H. Dodge, and B. Thelma Apolipoprotein E polymorphism and Alzheimer disease: the Indo-US cross-national dementia study Arch Neurol 57 2000 824
16. A.G. Gornall, C.J. Bardawill, and M.M. David Determination of serum proteins by means of the biuret reaction J Biol Chem 177 2 1949 751 766
17. L.C. Green, D.A. Wagner, J. Glogowski, P.L. Skipper, J.S. Wishnok, and S.R. Tannenbaum Analysis of nitrate, nitrite, and [15 N]nitrate in biological fluids Anal Biochem 126 1982 131 138
18. R. Hellweg, R. Nitsch, C. Hock, M. Jaksch, and S. Hoyer Nerve growth factor and choline acetyltransferase activity levels in the rat brain following experimental impairment of cerebral glucose and energy metabolism J Neurosci Res 31 1992 479 486
19. G.C. Jagetia, and T.K. Reddy Modulation of radiation-induced alteration in the antioxidant status of mice by naringin Life Sci 77 2005 780 794
20. G.C. Jagetia, V. Venkatesha, and T.K. Reddy Naringin, a citrus flavonone, protects against radiation-induced chromosome damage in mouse bone marrow Mutagenesis 18 2003 337 343
21. S.-M. Jeon, Y.B. Park, and M.-S. Choi Antihypercholesterolemic property of naringin alters plasma and tissue lipids, cholesterol-regulating enzymes, fecal sterol and tissue morphology in rabbits Clin Nutr 23 2004 1025 1034
22. D. Jollow, J. Mitchell, N. Zampaglione, and J. Gillette Bromobenzene-induced liver necrosis. Protective role of glutathione and evidence for 3, 4-bromobenzene oxide as the hepatotoxic metabolite Pharmacology 11 1974 151
23. A.D. Kandhare, K.S. Raygude, P. Ghosh, A.E. Ghule, and S.L. Bodhankar Neuroprotective effect of naringin by modulation of endogenous biomarkers in streptozotocin induced painful diabetic neuropathy Fitoterapia 83 2012 650 659
24. S.-i. Kanno, A. Shouji, A. Tomizawa, T. Hiura, Y. Osanai, and M. Ujibe Inhibitory effect of naringin on lipopolysaccharide (LPS)-induced endotoxin shock in mice and nitric oxide production in RAW 264.7 macrophages Life Sci 78 2006 673 681
25. A. Karam, A. Nadia, E.-F. Abd, A. Nemat, and M. Siham Protective Effect of Ginger (Zingiber officinale) on Alzheimer's disease Induced in Rats J Neuroinfect Dis 5 2014 2
26. H.-J. Kim, J.Y. Song, H.J. Park, H.-K. Park, D.H. Yun, and J.-H. Chung Naringin protects against rotenone-induced apoptosis in human neuroblastoma SH-SY5Y cells Korean J Physiol Pharmacol 13 2009 281 285
27. T.E. King Preparation of succinate dehydrogenase and reconstitution of succinate oxidase Methods Enzymol 10 1967 322 331
28. T.E. King, and R.L. Howard Preparations and properties of soluble NADH dehydrogenases from cardiac muscle Methods Enzymol 10 1967 275 294
29. A. Klugman, D.P. Naughton, M. Isaac, I. Shah, A. Petroczi, and N. Tabet Antioxidant enzymatic activities in Alzheimer's disease: the relationship to acetylcholinesterase inhibitors J Alzheimers Dis 30 2012 467 474
30. Y. Kono Generation of superoxide radical during autoxidation of hydroxylamine and an assay for superoxide dismutase Arch Biochem Biophys 186 1978 189 195
31. A. Kuhad, M. Bishnoi, V. Tiwari, and K. Chopra Suppression of NF-kappabeta signaling pathway by tocotrienol can prevent diabetes associated cognitive deficits Pharmacol Biochem Behav 92 2009 251 259
32. P. Kumar, and A. Kumar Protective effect of rivastigmine against 3-nitropropionic acid-induced Huntington's disease like symptoms: possible behavioural, biochemical and cellular alterations Eur J Pharmacol 615 2009 91 101
33. A. Kumar, S. Dogra, and A. Prakash Protective effect of naringin, a citrus flavonoid, against colchicine-induced cognitive dysfunction and oxidative damage in rats J Med Food 13 2010 976 984
34. P.G. Layer, R. Alber, and O. Sporns Quantitative Development and Molecular Forms of Acetyl and Butyrylcholinesterase During Morphogenesis and Synaptogenesis of Chick Brain and Retina J Neurochem 49 1987 175 182
35. S.R. Maratha, and N. Mahadevan Memory Enhancing Activity of Naringin in Unstressed and Stressed Mice: Possible Cholinergic and Nitriergic Modulation Neurochem Res 37 2012 2206 2212
36. S. Misra, V. Tiwari, A. Kuhad, and K. Chopra Modulation of nitrergic pathway by sesamol prevents cognitive deficits and associated biochemical alterations in intracerebroventricular streptozotocin administered rats Eur J Pharmacol 659 2011 177 186
37. P.I. Moreira, C. Carvalho, X. Zhu, M.A. Smith, and G. Perry Mitochondrial dysfunction is a trigger of Alzheimer's disease pathophysiology Biochim Biophys Acta 1802 2010 2 10
38. R. Morris, P. Garrud, J. Rawlins, and J. O'Keefe Place navigation impaired in rats with hippocampal lesions Nature 297 1982 681 683
39. T. Mosmann Rapid colorimetric assay for cellular growth and survival: application to proliferation and cytotoxicity assays J Immunol Methods 65 1983 55 63
40. T. Nakagami, N. Nanaumi-Tamura, K. Toyomura, T. Nakamura, and T. Shigehisa Dietary Flavonoids as Potential Natural Biological Response Modifiers Affecting the Autoimmune System J Food Sci 60 1995 653 656
41. R.J. Nijveldt, E. van Nood, D.E. van Hoorn, P.G. Boelens, K. van Norren, and P.A. van Leeuwen Flavonoids: a review of probable mechanisms of action and potential applications Am J Clin Nutr 74 2001 418 425
42. M. Rajadurai, and P. Prince Naringin ameliorates mitochondrial lipid peroxides, antioxidants and lipids in isoproterenol induced myocardial infarction in Wistar rats Phytother Res 23 2009 358 362
43. H. Raza, and A. John Streptozotocin-Induced Cytotoxicity, Oxidative Stress and Mitochondrial Dysfunction in Human Hepatoma HepG2 Cells Int J Mol Sci 13 2012 5751 5767
44. P.H. Reddy Mitochondrial dysfunction in aging and Alzheimer's disease: strategies to protect neurons Antioxid Redox Signal 9 2007 1647 1658
45. P.H. Reddy, and M.F. Beal Are mitochondria critical in the pathogenesis of Alzheimer's disease? Brain Res Brain Res Rev 49 2005 618 632
46. A.E. Reyes, D.R. Perez, A. Alvarez, J. Garrido, M.K. Gentry, and B.P. Doctor A monoclonal antibody against acetylcholinesterase inhibits the formation of amyloid fibrils induced by the enzyme Biochem Biophys Res Commun 232 1997 652 655
47. A.K. Sachdeva, A. Kuhad, V. Tiwari, V. Arora, and K. Chopra Protective Effect of Epigallocatechin Gallate in Murine Water Immersion Stress Model of Chronic Fatigue Syndrome Basic Clin Pharmacol Toxicol 106 2010 490 496
48. A.K. Sachdeva, A. Kuhad, and K. Chopra Epigallocatechin gallate ameliorates behavioral and biochemical deficits in rat model of load-induced chronic fatigue syndrome Brain Res Bull 86 2011 165 172
49. M. Salkovic-Petrisic, and S. Hoyer Central insulin resistance as a trigger for sporadic Alzheimer-like pathology: an experimental approach J Neural Transm Suppl 72 2007 217 233
50. M. Sharma, and Y. Gupta Effect of chronic treatment of melatonin on learning, memory and oxidative deficiencies induced by intracerebroventricular streptozotocin in rats Pharmacol Biochem Behav 70 2001 325 331
51. M. Sharma, and Y. Gupta Intracerebroventricular injection of streptozotocin in rats produces both oxidative stress in the brain and cognitive impairment Life Sci 68 2001 1021
52. M. Sharma, and Y. Gupta Chronic treatment with trans resveratrol prevents intracerebroventricular streptozotocin induced cognitive impairment and oxidative stress in rats Life Sci 71 2002 2489
53. D.P. Singh, and K. Chopra Flavocoxid, dual inhibitor of cyclooxygenase-2 and 5-lipoxygenase, exhibits neuroprotection in rat model of ischaemic stroke Pharmacol Biochem Behav 120 2014 33 42
54. F.V. So, N. Guthrie, A.F. Chambers, M. Moussa, and K.K. Carroll Inhibition of human breast cancer cell proliferation and delay of mammary tumorigenesis by flavonoids and citrus juices Nutr Cancer 26 1996 167 181
55. S. Sonkusare, K. Srinivasan, C. Kaul, and P. Ramarao Effect of donepezil and lercanidipine on memory impairment induced by intracerebroventricular streptozotocin in rats Life Sci 77 2005 1
56. G.L. Sottocasa, B. Kuylenstierna, L. Ernster, and A. Bergstrand An electron-transport system associated with the outer membrane of liver mitochondria. A biochemical and morphological study J Cell Biol 32 1967 415 438
57. N. Tabet Acetylcholinesterase inhibitors for Alzheimer's disease: anti-inflammatories in acetylcholine clothing! Age Ageing 35 2006 336 338
58. V. Tiwari, A. Kuhad, and K. Chopra Suppression of neuro-inflammatory signaling cascade by tocotrienol can prevent chronic alcohol-induced cognitive dysfunction in rats Behav Brain Res 203 2009 296 303
59. S. Tota, H. Awasthi, P.K. Kamat, C. Nath, and K. Hanif Protective effect of quercetin against intracerebral streptozotocin induced reduction in cerebral blood flow and impairment of memory in mice Behav Brain Res 209 2010 73
60. M. Tuzcu, and G. Baydas Effect of melatonin and vitamin E on diabetes-induced learning and memory impairment in rats Eur J Pharmacol 537 2006 106 110
61. E. Wills Mechanisms of lipid peroxide formation in animal tissues Biochem J 99 1966 667
62. N. Yassin, S. El-Shenawy, K.A. Mahdy, N. Gouda, A. Marrie, and A. Farrag Effect of Boswellia serrata on Alzheimer's disease induced in rats J Arab Soc Med Res 8 2013 1 11
63. V. Zbarsky, K.P. Datla, S. Parkar, D.K. Rai, O.I. Aruoma, and D.T. Dexter 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 39 2005 1119 1125
64. G. Zeevalk, L. Bernard, C. Song, M. Gluck, and J. Ehrhart Mitochondrial inhibition and oxidative stress: reciprocating players in neurodegeneration Antioxid Redox Signal 7 2005 1117 1139