Chronic administration of quercetin prevent spatial learning and memory deficits provoked by chronic stress in rats

Behavioural Brain Research

Volumn 270, Issue , 2014, Pages 196-205

  Said Mohammadi, Hadis ^a   Goudarzi, Iran ^a   Lashkarbolouki, Taghi ^a   Abrari, Kataneh ^a   Elahdadi Salmani, Mahmoud ^a  

^a DAMGHAN UNIVERSITY   (Iran)

Author keywords

Chronic stress; Oxidative stress; Quercetin; Rat; Spatial memory

Indexed keywords

CORTICOSTERONE; GLUTATHIONE PEROXIDASE; MALONALDEHYDE; QUERCETIN; SUPEROXIDE DISMUTASE; ANTIOXIDANT;

AMNESIA; ANALYSIS OF VARIANCE; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIOXIDANT ACTIVITY; ARTICLE; CHRONIC STRESS; COGNITION; CONTROLLED STUDY; CORTICOSTERONE BLOOD LEVEL; DIET THERAPY; ENZYME ACTIVITY; HIPPOCAMPUS; IMMOBILIZATION STRESS; LATENT PERIOD; MEMORY CONSOLIDATION; MORRIS WATER MAZE TEST; NEUROPROTECTION; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; PROBE TEST; RAT; SPATIAL LEARNING; TRAINING; ANIMAL; BLOOD; COMPLICATION; DRUG EFFECTS; EXERCISE; MALE; MAZE TEST; MEMORY DISORDERS; MENTAL STRESS; METABOLISM; NEUROPSYCHOLOGICAL TEST; PROCEDURES; PSYCHOLOGY; SPATIAL MEMORY; TIME; TREATMENT OUTCOME; WISTAR RAT;

ANIMALS; ANTIOXIDANTS; CORTICOSTERONE; GLUTATHIONE PEROXIDASE; HIPPOCAMPUS; MALE; MALONDIALDEHYDE; MAZE LEARNING; MEMORY DISORDERS; NEUROPSYCHOLOGICAL TESTS; QUERCETIN; RATS; RATS, WISTAR; RESTRAINT, PHYSICAL; SPATIAL LEARNING; SPATIAL MEMORY; STRESS, PSYCHOLOGICAL; SUPEROXIDE DISMUTASE; TIME FACTORS; TREATMENT OUTCOME;

EID: 84901481027     PISSN: 01664328     EISSN: 18727549     Source Type: Journal    
DOI: 10.1016/j.bbr.2014.05.015     Document Type: Article

References (97)

1. Kolber B.J., Wieczorek L., Muglia L.J. Hypothalamic-pituitary-adrenal axis dysregulation and behavioral analysis of mouse mutants with altered glucocorticoid or mineralocorticoid receptor function. Stress 2008, 11:321-338.
2. Kim J.J., Song E.Y., Kosten T.A. Stress effects in the hippocampus: synaptic plasticity and memory. Stress 2006, 9:1-11.
3. Lupien S.J., Lepage M. Stress, memory, and the hippocampus: can't live with it, can't live without it. Behavioural Brain Research 2001, 127:137-158.
4. McEwen B.S. The neurobiology of stress: from serendipity to clinical relevance. Brain Research 2000, 886:172-189.
5. De Kloet E.R., Vreugdenhil E., Oitzl M.S., Joels M. Brain corticosteroid receptor balance in health and disease. Endocrine Reviews 1998, 19:269-301.
6. Bremner J.D. Stress and brain atrophy. CNS & Neurological Disorders Drug Targets 2006, 5:503-512.
7. Conrad C.D. What is the functional significance of chronic stress-induced CA3 dendritic retraction within the hippocampus. Behavioral and Cognitive Neuroscience Reviews 2006, 5:41-60.
8. Lucassen P.J., Heine V.M., Muller M.B., van der Beek E.M., Wiegant V.M., De Kloet E.R., et al. Stress, depression and hippocampal apoptosis. CNS & Neurological Disorders Drug Targets 2006, 5:531-546.
9. Joels M., Karst H., Alfarez D., Heine V.M., Qin Y., van Riel E., et al. Effects of chronic stress on structure and cell function in rat hippocampus and hypothalamus. Stress 2004, 7:221-231.
10. Sapolsky R.M. Stress and plasticity in the limbic system. Neurochemical Research 2003, 28:1735-1742.
11. Vasconcellos A.P., Tabajara A.S., Ferrari C., Rocha E., Dalmaz C. Effect of chronic stress on spatial memory in rats is attenuated by lithium treatment. Physiology & Behavior 2003, 79:143-149.
12. Srikumar B.N., Raju T.R., Shankaranarayana Rao B.S. Contrasting effects of bromocriptine on learning of a partially baited radial arm maze task in the presence and absence of restraint stress. Psychopharmacology (Berl) 2007, 193:363-374.
13. Orsetti M., Colella L., Dellarole A., Canonico P.L., Ghi P. Modification of spatial recognition memory and object discrimination after chronic administration of haloperidol, amitriptyline, sodium valproate or olanzapine in normal and anhedonic rats. The International Journal of Neuropsychopharmacology/Official Scientific Journal of the Collegium Internationale Neuropsychopharmacologicum. 2007, 10:345-357.
14. Ghadrdoost B., Vafaei A.A., Rashidy-Pour A., Hajisoltani R., Bandegi A.R., Motamedi F., et al. Protective effects of saffron extract and its active constituent crocin against oxidative stress and spatial learning and memory deficits induced by chronic stress in rats. European Journal of Pharmacology 2011, 667:222-229.
15. Cumurcu B.E., Ozyurt H., Etikan I., Demir S., Karlidag R. Total antioxidant capacity and total oxidant status in patients with major depression: impact of antidepressant treatment. Psychiatry and Clinical Neurosciences 2009, 63:639-645.
16. Lucca G., Comim C.M., Valvassori S.S., Reus G.Z., Vuolo F., Petronilho F., et al. Effects of chronic mild stress on the oxidative parameters in the rat brain. Neurochemistry International 2009, 54:358-362.
17. Madrigal J.L., Olivenza R., Moro M.A., Lizasoain I., Lorenzo P., Rodrigo J., et al. Glutathione depletion, lipid peroxidation and mitochondrial dysfunction are induced by chronic stress in rat brain. Neuropsychopharmacology: Official Publication of the American College of Neuropsychopharmacology 2001, 24:420-429.
18. Olivenza R., Moro M.A., Lizasoain I., Lorenzo P., Fernandez A.P., Rodrigo J., et al. Chronic stress induces the expression of inducible nitric oxide synthase in rat brain cortex. Journal of Neurochemistry 2000, 74:785-791.
19. Sato H., Takahashi T., Sumitani K., Takatsu H., Urano S. Glucocorticoid generates ROS to induce oxidative injury in the hippocampus, leading to impairment of cognitive function of rats. Journal of Clinical Biochemistry and Nutrition 2010, 47:224-232.
20. Poon H.F., Calabrese V., Scapagnini G., Butterfield D.A. Free radicals and brain aging. Clinics in Geriatric Medicine 2004, 20:329-359.
21. Uttara B., Singh A.V., Zamboni P., Mahajan R.T. Oxidative stress and neurodegenerative diseases: a review of upstream and downstream antioxidant therapeutic options. Current Neuropharmacology 2009, 7:65-74.
22. Tsang A.H., Chung K.K. Oxidative and nitrosative stress in Parkinson's disease. Biochimica et Biophysica Acta 2009, 1792:643-650.
23. Goldberg D.M., Hahn S.E., Parkes J.G. Beyond alcohol: beverage consumption and cardiovascular mortality. Clinica Chimica Acta; International Journal of Clinical Chemistry 1995, 237:155-187.
24. Sampson L., Rimm E., Hollman P.C., de Vries J.H., Katan M.B. Flavonol and flavone intakes in US health professionals. Journal of the American Dietetic Association 2002, 102:1414-1420.
25. Saponara S., Sgaragli G., Fusi F. Quercetin as a novel activator of L-type Ca(2+) channels in rat tail artery smooth muscle cells. British Journal of Pharmacology 2002, 135:1819-1827.
26. Chander V., Singh D., Chopra K. Reversal of experimental myoglobinuric acute renal failure in rats by quercetin, a bioflavonoid. Pharmacology 2005, 73:49-56.
27. Nagata H., Takekoshi S., Takagi T., Honma T., Watanabe K. Antioxidative action of flavonoids, quercetin and catechin, mediated by the activation of glutathione peroxidase. The Tokai Journal of Experimental and Clinical Medicine 1999, 24:1-11.
28. Spencer J.P. Food for thought: the role of dietary flavonoids in enhancing human memory, learning and neuro-cognitive performance. The Proceedings of the Nutrition Society 2008, 67:238-252.
29. Spencer J.P. Flavonoids: modulators of brain function?. The British Journal of Nutrition 2008, 99(E Suppl 1):ES60-ES77.
30. Shukitt-Hale B., Lau F.C., Joseph J.A. Berry fruit supplementation and the aging brain. Journal of Agricultural and Food Chemistry 2008, 56:636-641.
31. Shukitt-Hale B., Carey A.N., Jenkins D., Rabin B.M., Joseph J.A. Beneficial effects of fruit extracts on neuronal function and behavior in a rodent model of accelerated aging. Neurobiology of Aging 2007, 28:1187-1194.
32. Wang Y., Wang L., Wu J., Cai J. The in vivo synaptic plasticity mechanism of EGb 761-induced enhancement of spatial learning and memory in aged rats. British Journal of Pharmacology 2006, 148:147-153.
33. Joseph J.A., Shukitt-Hale B., Denisova N.A., Bielinski D., Martin A., McEwen J.J., et al. Reversals of age-related declines in neuronal signal transduction, cognitive, and motor behavioral deficits with blueberry, spinach, or strawberry dietary supplementation. The Journal of Neuroscience: The Official Journal of the Society for Neuroscience 1999, 19:8114-8121.
34. Shif O., Gillette K., Damkaoutis C.M., Carrano C., Robbins S.J., Hoffman J.R. Effects of Ginkgo biloba administered after spatial learning on water maze and radial arm maze performance in young adult rats. Pharmacology, Biochemistry, and Behavior 2006, 84:17-25.
35. Hartman R.E., Shah A., Fagan A.M., Schwetye K.E., Parsadanian M., Schulman R.N., et al. Pomegranate juice decreases amyloid load and improves behavior in a mouse model of Alzheimer's disease. Neurobiology of Disease 2006, 24:506-515.
36. Winter J.C. The effects of an extract of Ginkgo biloba, EGb 761, on cognitive behavior and longevity in the rat. Physiology & Behavior 1998, 63:425-433.
37. Haque A.M., Hashimoto M., Katakura M., Tanabe Y., Hara Y., Shido O. Long-term administration of green tea catechins improves spatial cognition learning ability in rats. The Journal of Nutrition 2006, 136:1043-1047.
38. van Praag H., Lucero M.J., Yeo G.W., Stecker K., Heivand N., Zhao C., et al. Plant-derived flavanol (-)epicatechin enhances angiogenesis and retention of spatial memory in mice. The Journal of Neuroscience: The Official Journal of the Society for Neuroscience 2007, 27:5869-5878.
39. Kawabata K., Kawai Y., Terao J. Suppressive effect of quercetin on acute stress-induced hypothalamic-pituitary-adrenal axis response in Wistar rats. The Journal of Nutritional Biochemistry 2010, 21:374-380.
40. Selvakumar K., Bavithra S., Suganthi M., Benson C.S., Elumalai P., Arunkumar R., et al. Protective role of quercetin on PCBs-induced oxidative stress and apoptosis in hippocampus of adult rats. Neurochemical Research 2012, 37:708-721.
41. Mahesh T., Menon V.P. Quercetin allievates oxidative stress in streptozotocin-induced diabetic rats. Phytotherapy Research: PTR. 2004, 18:123-127.
42. Erden Inal M., Kahraman A. The protective effect of flavonol quercetin against ultraviolet a induced oxidative stress in rats. Toxicology 2000, 154:21-29.
43. Enache M., Van Waes V., Vinner E., Lhermitte M., Maccari S., Darnaudery M. Impact of an acute exposure to ethanol on the oxidative stress status in the hippocampus of prenatal restraint stress adolescent male rats. Brain Research 2008, 1191:55-62.
44. Ohkawa H., Ohishi N., Yagi K. Assay for lipid peroxides in animal tissues by thiobarbituric acid reaction. Analytical Biochemistry 1979, 95:351-358.
45. Becana M., Aparicio-Tejo P., Irigoyen J.J., Sanchez-Diaz M. Some enzymes of hydrogen peroxide metabolism in leaves and root nodules of Medicago sativa. Plant Physiology 1986, 82:1169-1171.
46. Wendel A. Glutathione peroxidase. Methods in Enzymology 1981, 77:325-333.
47. Lowry O.H., Rosebrough N.J., Farr A.L., Randall R.J. Protein measurement with the Folin phenol reagent. The Journal of Biological Chemistry 1951, 193:265-275.
48. McLaughlin K.J., Gomez J.L., Baran S.E., Conrad C.D. The effects of chronic stress on hippocampal morphology and function: an evaluation of chronic restraint paradigms. Brain Research 2007, 1161:56-64.
49. Kleen J.K., Sitomer M.T., Killeen P.R., Conrad C.D. Chronic stress impairs spatial memory and motivation for reward without disrupting motor ability and motivation to explore. Behavioral Neuroscience 2006, 12:842-851.
50. Song L., Che W., Min-Wei W., Murakami Y., Matsumoto K. Impairment of the spatial learning and memory induced by learned helplessness and chronic mild stress. Pharmacology, Biochemistry, and Behavior 2006, 83:186-193.
51. Sandi C., Davies H.A., Cordero M.I., Rodriguez J.J., Popov V.I., Stewart M.G. Rapid reversal of stress induced loss of synapses in CA3 of rat hippocampus following water maze training. The European Journal of Neuroscience 2003, 17:2447-2456.
52. Conrad C.D., Galea L.A., Kuroda Y., McEwen B.S. Chronic stress impairs rat spatial memory on the Y maze, and this effect is blocked by tianeptine pretreatment. Behavioral Neuroscience 1996, 110:1321-1334.
53. Leuner B., Gould E., Shors T.J. Is there a link between adult neurogenesis and learning. Hippocampus 2006, 16:216-224.
54. Astur R.S., Taylor L.B., Mamelak A.N., Philpott L., Sutherland R.J. Humans with hippocampus damage display severe spatial memory impairments in a virtual Morris water task. Behavioural Brain Research 2002, 132:77-84.
55. Kessels R.P., de Haan E.H., Kappelle L.J., Postma A. Varieties of human spatial memory: a meta-analysis on the effects of hippocampal lesions. Brain Research Brain Research Reviews 2001, 35:295-303.
56. King J.A., Burgess N., Hartley T., Vargha-Khadem F., O'Keefe J. Human hippocampus and viewpoint dependence in spatial memory. Hippocampus 2002, 12:811-820.
57. Joels M., Karst H., Krugers H.J., Lucassen P.J. Chronic stress: implications for neuronal morphology, function and neurogenesis. Frontiers in Neuroendocrinology 2007, 28:72-96.
58. Kim J.J., Diamond D.M. The stressed hippocampus, synaptic plasticity and lost memories. Nature Reviews Neuroscience 2002, 3:453-462.
59. Stewart M.G., Davies H.A., Sandi C., Kraev I.V., Rogachevsky V.V., Peddie C.J., et al. Stress suppresses and learning induces plasticity in CA3 of rat hippocampus: a three-dimensional ultrastructural study of thorny excrescences and their postsynaptic densities. Neuroscience 2005, 131:43-54.
60. McEwen B.S. Effects of adverse experiences for brain structure and function. Biological Psychiatry 2000, 48:721-731.
61. McEwen B.S. Plasticity of the hippocampus: adaptation to chronic stress and allostatic load. Annals of the New York Academy of Sciences 2001, 933:265-277.
62. Simmons H.F., James R.C., Harbison R.D., Patel D.G., Roberts S.M. Examination of the role of catecholamines in hepatic glutathione suppression by cold-restraint in mice. Toxicology 1991, 67:29-40.
63. Perez-Nievas B.G., Garcia-Bueno B., Caso J.R., Menchen L., Leza J.C. Corticosterone as a marker of susceptibility to oxidative/nitrosative cerebral damage after stress exposure in rats. Psychoneuroendocrinology 2007, 32:703-711.
64. Cohen-Kerem R., Koren G. Antioxidants and fetal protection against ethanol teratogenicity. I. Review of the experimental data and implications to humans. Neurotoxicology and Teratology 2003, 25:1-9.
65. McIntosh L.J., Sapolsky R.M. Glucocorticoids increase the accumulation of reactive oxygen species and enhance adriamycin-induced toxicity in neuronal culture. Experimental Neurology 1996, 141:201-206.
66. Amoroso S., D'Alessio A., Sirabella R., Di Renzo G., Annunziato L. Ca(2+)-independent caspase-3 but not Ca(2+)-dependent caspase-2 activation induced by oxidative stress leads to SH-SY5Y human neuroblastoma cell apoptosis. Journal of Neuroscience Research 2002, 68:454-462.
67. Kroemer G. The proto-oncogene Bcl-2 and its role in regulating apoptosis. Nature Medicine 1997, 3:614-620.
68. Cregan S.P., Fortin A., MacLaurin J.G., Callaghan S.M., Cecconi F., Yu S.W., et al. Apoptosis-inducing factor is involved in the regulation of caspase-independent neuronal cell death. The Journal of Cell Biology 2002, 158:507-517.
69. Stojiljkovic V., Todorovic A., Kasapovic J., Pejic S., Pajovic S.B. Antioxidant enzyme activity in rat hippocampus after chronic and acute stress exposure. Annals of the New York Academy of Sciences 2005, 1048:373-376.
70. Zaidi S.M., Banu N. Antioxidant potential of vitamins A, E and C in modulating oxidative stress in rat brain. Clinica Chimica Acta; International Journal of Clinical Chemistry 2004, 340:229-233.
71. Walesiuk A., Trofimiuk E., Braszko J.J. Ginkgo biloba normalizes stress- and corticosterone-induced impairment of recall in rats. Pharmacological Research: The Official Journal of the Italian Pharmacological Society 2006, 53:123-128.
72. Zafir A., Banu N. Antioxidant potential of fluoxetine in comparison to Curcuma longa in restraint-stressed rats. European Journal of Pharmacology 2007, 572:23-31.
73. Zafir A.B.N. Induction of oxidative stress by restraint stress and corticosterone treatment in rats. Indian Journal of Biochemistry & Biophysics 2009, 46:53-58.
74. Yao Y., Han D.D., Zhang T., Yang Z. Quercetin improves cognitive deficits in rats with chronic cerebral ischemia and inhibits voltage-dependent sodium channels in hippocampal CA1 pyramidal neurons. Phytotherapy Research: PTR 2010, 24:136-140.
75. Tota S., Awasthi H., Kamat P.K., Nath C., Hanif K. Protective effect of quercetin against intracerebral streptozotocin induced reduction in cerebral blood flow and impairment of memory in mice. Behavioural Brain Research 2010, 209:73-79.
76. Sharma D.R., Wani W.Y., Sunkaria A., Kandimalla R.J., Verma D., Cameotra S.S., et al. Quercetin protects against chronic aluminum-induced oxidative stress and ensuing biochemical, cholinergic, and neurobehavioral impairments in rats. Neurotoxicity Research 2013, 23:336-357.
77. Su Wen Sun H.Q.Y., Hong Zhang, Yuan Lin Zheng, Jian Jun Wang, Lan Luo. Quercetin attenuates spontaneous behavior and spatial memory impairment in d-galactose-treated mice by increasing brain antioxidant capacity. Nutrition Research 2007, 27:169-175.
78. Bhutada P., Mundhada Y., Bansod K., Bhutada C., Tawari S., Dixit P., et al. Ameliorative effect of quercetin on memory dysfunction in streptozotocin-induced diabetic rats. Neurobiology of Learning and Memory 2010, 94:293-302.
79. Stein-Behrens B., Mattson M.P., Chang I., Yeh M., Sapolsky R. Stress exacerbates neuron loss and cytoskeletal pathology in the hippocampus. The Journal of Neuroscience: The Official Journal of the Society for Neuroscience 1994, 14:5373-5380.
80. McIntosh L.J., Hong K.E., Sapolsky R.M. Glucocorticoids may alter antioxidant enzyme capacity in the brain: baseline studies. Brain Research 1998, 791:209-214.
81. Massaad C.A., Klann E. Reactive oxygen species in the regulation of synaptic plasticity and memory. Antioxidants & Redox Signaling 2011, 14:2013-2054.
82. Dumont M., Wille E., Stack C., Calingasan N.Y., Beal M.F., Lin M.T. Reduction of oxidative stress, amyloid deposition, and memory deficit by manganese superoxide dismutase overexpression in a transgenic mouse model of Alzheimer's disease. FASEB Journal: Official Publication of the Federation of American Societies for Experimental Biology 2009, 23:2459-2466.
83. Bickford P.C., Gould T., Briederick L., Chadman K., Pollock A., Young D., et al. Antioxidant-rich diets improve cerebellar physiology and motor learning in aged rats. Brain Research 2000, 866:211-217.
84. Cui K., Luo X., Xu K., Ven Murthy M.R. Role of oxidative stress in neurodegeneration: recent developments in assay methods for oxidative stress and nutraceutical antioxidants. Progress in Neuro-psychopharmacology & Biological Psychiatry 2004, 28:771-799.
85. Gutteridge J.M. Lipid peroxidation and antioxidants as biomarkers of tissue damage. Clinical Chemistry 1995, 41:1819-1828.
86. Mattson M.P., Keller J.N., Begley J.G. Evidence for synaptic apoptosis. Experimental Neurology 1998, 153:35-48.
87. Esterbauer H., Schaur R.J., Zollner H. Chemistry and biochemistry of 4-hydroxynonenal, malonaldehyde and related aldehydes. Free Radical Biology & Medicine 1991, 11:81-128.
88. Fontella F.U., Siqueira I.R., Vasconcellos A.P., Tabajara A.S., Netto C.A., Dalmaz C. Repeated restraint stress induces oxidative damage in rat hippocampus. Neurochemical Research 2005, 30:105-111.
89. Fukui K., Omoi N.O., Hayasaka T., Shinnkai T., Suzuki S., Abe K., et al. Cognitive impairment of rats caused by oxidative stress and aging, and its prevention by vitamin E. Annals of the New York Academy of Sciences 2002, 959:275-284.
90. Gispen W.H., Biessels G.J. Cognition and synaptic plasticity in diabetes mellitus. Trends in Neurosciences 2000, 23:542-549.
91. Boots A.W., Haenen G.R., Bast A. Health effects of quercetin: from antioxidant to nutraceutical. European Journal of Pharmacology 2008, 585:325-337.
92. Hanasaki Y., Ogawa S., Fukui S. The correlation between active oxygens scavenging and antioxidative effects of flavonoids. Free Radical Biology & Medicine 1994, 16:845-850.
93. Patel R., McIntosh L., McLaughlin J., Brooke S., Nimon V., Sapolsky R. Disruptive effects of glucocorticoids on glutathione peroxidase biochemistry in hippocampal cultures. Journal of Neurochemistry 2002, 82:118-125.
94. Singh A., Naidu P.S., Kulkarni S.K. Reversal of aging and chronic ethanol-induced cognitive dysfunction by quercetin a bioflavonoid. Free Radical Research 2003, 37:1245-1252.
95. Liu J., Yu H., Ning X. Effect of quercetin on chronic enhancement of spatial learning and memory of mice. Science in China Series C, Life sciences/Chinese Academy of Sciences 2006, 49:583-590.
96. Kuo S.M., Leavitt P.S., Lin C.P. Dietary flavonoids interact with trace metals and affect metallothionein level in human intestinal cells. Biological Trace Element Research 1998, 62:135-153.
97. Bolanos J.P., Almeida A., Stewart V., Peuchen S., Land J.M., Clark J.B., et al. Nitric oxide-mediated mitochondrial damage in the brain: mechanisms and implications for neurodegenerative diseases. Journal of Neurochemistry 1997, 68:2227-2240.