Memory enhancing effects of saffron in aged mice are correlated with antioxidant protection

Behavioural Brain Research

Volumn 219, Issue 2, 2011, Pages 197-204

  Papandreou, Magdalini A ^a   Tsachaki, Maria ^b   Efthimiopoulos, Spiros ^b   Cordopatis, Paul ^a   Lamari, Fotini N ^a   Margarity, Marigoula ^a  

^a UNIVERSITY OF PATRAS   (Greece)

^b UNIVERSITY OF ATHENS   (Greece)

Author keywords

Acetylcholinesterase; Aging; Crocetin; Free radicals; Learning memory; Oxidative stress; Saffron; Safranal; SH SY5Y

Indexed keywords

ACETYLCHOLINESTERASE; ANTIOXIDANT; CASPASE 3; CROCETIN; NOOTROPIC AGENT; REACTIVE OXYGEN METABOLITE; SAFFRON; SAFRANAL; UNCLASSIFIED DRUG;

AGING; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIOXIDANT ACTIVITY; ARTICLE; BAGG ALBINO MOUSE; BRAIN HOMOGENATE; BRAIN PROTECTION; CELL STRAIN; CELL STRAIN SH SY5Y; CELL VIABILITY; CEREBELLUM; COGNITION; CONTROLLED STUDY; DRUG EFFECT; ENZYME ACTIVATION; ENZYME ACTIVITY; HUMAN; HUMAN CELL; LEARNING; MALE; MEMORY; MENTAL PERFORMANCE; MOUSE; NEUROBLASTOMA CELL; NONHUMAN; OXIDATIVE STRESS; PASSIVE AVOIDANCE; PRIORITY JOURNAL; TREATMENT DURATION;

ACETYLCHOLINESTERASE; AGING; ANIMALS; ANTIOXIDANTS; AVOIDANCE LEARNING; BRAIN CHEMISTRY; CAROTENOIDS; CASPASE 3; CELL LINE, TUMOR; CELL SURVIVAL; CROCUS; ENZYME ACTIVATION; HUMANS; HYDROGEN PEROXIDE; INJECTIONS, INTRAPERITONEAL; LEARNING; MALE; MEMORY; MICE; MICE, INBRED BALB C; OXIDANTS; PLANT EXTRACTS; REACTIVE OXYGEN SPECIES;

EID: 79952707829     PISSN: 01664328     EISSN: 18727549     Source Type: Journal    
DOI: 10.1016/j.bbr.2011.01.007     Document Type: Article

References (80)

1. Abe K., Sugiura M., Yamaguchi S., Shoyama Y., Saito H. Saffron extract prevents acetaldehyde-induced inhibition of long term potentiation in the rat dentate gyrus in vivo. Brain Res 1999, 851:287-289.
2. Ahmad A.S., Ansari M.A., Ahmad M., Saleem S., Yousuf S., Hoda M.N., et al. Neuroprotection by crocetin in a hemi-parkinsonan rat model. Pharmacol Biochem Behav 2005, 81:805-813.
3. Akhondzadeh S., Shafiee Sabet M., Harirchian M.H., Togha M., Cheraghmakani H., Razeghi S., et al. A 22-week, multicenter, randomized, double-blind controlled trial of Crocus sativus in the treatment of mild-to-moderate Alzheimer's disease. Psychopharmacol (Berl) 2010, 207:637-643.
4. Asai A., Nakano T., Takahashi M., Nagao A. Orally administered crocetin and crocins are absorbed into blood plasma as crocetin and its glucuronide conjugates in mice. J Agric Food Chem 2005, 53:7302-7306.
5. Bartus R.T., Dean R.L., Beer B., Lippa A.S. The cholinergic hypothesis of geriatric memory dysfunction. Science 1982, 217:408-414.
6. Benzie I.F.F., Strain J.J. The ferric reducing ability of plasma as a measure of " antioxidant power: the FRAP assay. Anal Biochem 1996, 239:70-76.
7. Birthelmer A., Stemmelin J., Jackish R., Cassel J.C. Presynaptic modulation of acetylcholine, noradrenaline and serotonin release in the hippocampus of aged rats with various levels of memory impairments. Brain Res Bull 2003, 60:283-296.
8. Butterfield D.A., Abdul H.M., Newman S., Reed T. Redox proteomics in some age-related neurodegenerative disorders or models thereof. NeuroRx 2006, 3:344-357.
9. Collerton D. Cholinergic function and intellectual decline in Alzheimer's disease. Neuroscience 1986, 19:1-28.
10. Darreh-Shori T., Meurling L., Pettersson T., Hugosson K., Hellström-Lindahl E., Andreasen N., et al. Changes in the activity and protein levels of CSF acetylcholinesterases in relation to cognitive function of patients with mild Alzheimer's disease following chronic donepezil treatment. J Neural Transm 2006, 113:1791-1801.
11. Das A., Dikshit M., Nath C. Role of molecular isoforms of acetylcholinesterase in learning and memory functions. Pharmacol Biochem Behav 2005, 81:89-99.
12. Das A., Dikshit M., Nath C. Profile of acetylcholinesterase in brain areas of male and female rats of adult and old age. Life Sci 2001, 68:1545-1555.
13. De Lacalle S., Iraizoz I., MaGonzalo L. Differential changes in cell size and number in topographic subdivisions of human basal nucleus in normal aging. Neuroscience 1991, 43:445-456.
14. Ellman G.L., Courtney K.D., Andres V., Featherstone R.M. A new and rapid colorimetric determination of acetyl cholinesterase activity. Biochem Pharmacol 1961, 7:88-95.
15. Fisher W., Nilsson O.G., Sjorklund A. In vitro acetylcholine release as measured by microdialysis is unaltered in the hippocampus of cognitively impaired aged rats with degenerative changes in the basal forebrain. Brain Res 1991, 556:44-52.
16. Forster M.J., Dubey A., Dawson K.M., Stutts W.A., Lal H., Sohal R.S. Age-related losses of cognitive function and motor skills in mice are associated with oxidative protein damage in the brain. Proc Natl Acad Sci USA 1996, 93:4765-4769.
17. Gallagher M., Colombo P.J. Ageing: the cholinergic hypothesis of cognitive decline. Curr Opin Neurobiol 1995, 5:161-168.
18. Gallagher M. Issues in the development of models for cognitive aging across primate and non-primate species. Neurobiol Aging 1993, 14:631-633.
19. Giaccio M. Crocetin from saffron: an active component of an ancient spice. Crit Rev Food Sci Nutr 2004, 44:155-172.
20. Gorini A., Ghingini B., Villa R.F. Acetylcholinesterase activity of synaptic plasma membranes during aging: effect of l-acetylcarnitine. Dementia 1996, 7:147-154.
21. Govoni S., Amadio M., Battaini F., Pascale A. Senescence of the brain: focus on cognitive kinases. Curr Pharm Des 2010, 16:660-671.
22. Grotto D., Santa Maria L.D., Boeira S., Valentini J., Charão M.F., Moro A.M., et al. Rapid quantification of malondialdehyde in plasma by high performance liquid chromatography-visible detection. J Pharm Biomed Anal 2007, 43:619-624.
23. Hollander J., Barrows C.H. Enzymatic studies in senescent rodent brains. J Gerontol 1968, 23:174-179.
24. Hosseinzadeh H., Sadeghnia H.R., Ziaee T., Danaee A. Protective effect of aqueous saffron extract (Crocus sativus L.) and crocin, its active constituent, on renal ischemia-reperfusion-induced oxidative damage in rats. J Pharm Pharm Sci 2005, 8:387-393.
25. Jayakumar T., Thomas P.A., Geraldine P. Protective effect of an extract of the oyster mushroom Pleurotus ostreatus, on antioxidants of major organs of aged rats. J Phys Chem B 2007, 111:7978-7986.
26. Jentzsch A.M., Bachmann H., Fürst P., Biesalski H.K. Improved analysis of malondialdehyde in human body fluids. Free Radic Biol Med 1996, 20:251-256.
27. Kameyama T., Nabeshima T., Kozawa T. Step-down-type passive avoidance- and escape-learning method Suitability for experimental amnesia models. J Pharmacol Methods 1986, 16:39-52.
28. Kanakis C.D., Tarantilis P.A., Tajmir-Riahi H.A., Polissiou M.G. Crocetin, dimethylcrocetin, and safranal bind human serum albumin: stability and antioxidative properties. J Agric Food Chem 2007, 55:970-977.
29. Kaneto H. Learning/memory processes under stress conditions. Behav Brain Res 1997, 83:71-74.
30. Kaur T., Pathak C.M., Pandhi P., Khanduja K.L. Effects of green tea extract on learning, memory, behaviour and acetylcholinesterase activity in young and old male rats. Brain Cogn 2008, 67:25-30.
31. Kuhl D.E., Koeppe R.A., Minoshima S., Snyder S.E., Ficaro E.P., Foster N.L., et al. In vivo mapping of cerebral acetylcholinesterase activity in aging and Alzheimer's disease. Neurology 1999, 52:691-699.
32. Lams B.E., Isacson O., Sofroniew M.V. Loss of transmitter-associated enzyme staining following axotomy does not indicate death of brainstem cholinergic neurons. Brain Res 1988, 475:401-406.
33. Lane R.M., Potkin S.G., Enz A. Targeting acetylcholinesterase and butyrylcholinesterase in dementia. Int J Neuropsychopharmacol 2006, 9:101-124.
34. Martorana A., Esposito Z., Koch G. Beyond the cholinergic hypothesis: do current drugs work in Alzheimer's disease?. CNS Neurosci Ther 2010, 16:235-245.
35. McGeer P.L., McGeer E.G., Suzuki J., Dolman C.E., Nagai T. Aging, Alzheimer's disease and the cholinergic system of basal forebrain. Neurology 1984, 34:741-745.
36. McGeer P.L., McGeer E.G., Singh V.K., Chase W.H. Choline acetyltransferase localization in the central nervous system by immunohistochemistry. Brain Res 1974, 81:373-379.
37. McGeer E.G., Fibiger H.C., McGeer P.L., Wilckson V. Aging and brain enzymes. Exp Gerontol 1971, 6:391-396.
38. McKinney M., Jacksonville M.C. Brain cholinergic vulnerability: relevance to behavior and disease. Biochem Pharmacol 2005, 70:1115-1124.
39. Meneguz A., Bisso G.M., Michalek H. Age-related changes in acetylcholinesterase and its molecular forms in various brain areas of rats. Neurochem Res 1992, 17:785-790.
40. Mokrasch L.C., Teschke E.J. Glutathione content of cultured cells and rodent brain regions: a specific fluorometric assay. Anal Biochem 1984, 140:506-509.
41. 2 modifies membrane structure and activity of acetylcholinesterase. Chem Biol Interact 2005, 157(158):401-404.
42. Moudgil V.K., Kanungo M.S. Effect of age on the circadian rhythm of acetylcholinesterase of the brain of the rat. Comp Gen Pharmacol 1973, 4:127-130.
43. Moyano S., Del Rio J., Frechilla D. Role of hippocampal CaMKII in serotonin 5-HT(1) receptor-mediated learning deficits in rats. Neuropsychopharmacology 2004, 29:2216-2224.
44. Murali G., Panneerselvam C. Age-associated oxidative macromolecular damages in rat brain regions: role of glutathione monoester. J Gerontol A: Biol Sci Med Sci 2007, 62:824-830.
45. Nichols N.R., Day J.R., Laping N.J., Johnson S.A., Finch C.E. GFAP mRNA increases with age in rat and human brain. Neurobiol Aging 1993, 14:421-429.
46. Nicolle M.M., Gonzalez J., Sugaya K., Baskerville K.A., Bryan D., Lund K., et al. Signatures of hippocampal oxidative stress in aged spatial learning-impaired rodents. Neuroscience 2001, 107:415-431.
47. Ochiai T., Ohno S., Soeda S., Tanaka H., Shoyama Y., Shimeno H. Crocin prevents the death of rat pheochromyctoma (PC-12) cells by its antioxidant effects stronger than those of alpha-tocopherol. Neurosci Lett 2004, 362:61-64.
48. Ochiai T., Soeda S., Ohno S., Tanaka H., Shoyama Y., Shimeno H. Crocin prevents the death of PC-12 cells through sphingomyelinase-ceramide signalling by increasing glutathione synthesis. Neurochem Int 2004, 44:321-330.
49. Ochiai T., Shimeno H., Mishima K., Iwasaki K., Fujiwara M., Tanaka H., et al. Protective effects of carotenoids from saffron on neuronal injury in vitro and in vivo. Biochim Biophys Acta 2007, 1770:578-584.
50. Otano A., Garcia-Osta A., Ballaz S., Frechilla D., Del Rio J. Facilitation by 8-OH-DPAT of passive avoidance performance in rats after inactivation of 5-HT(1A) receptors. Brain. J Pharmacol 1999, 128:1691-1698.
51. Ordoudi S.A., Befani C.D., Nenadis N., Koliakos G.G., Tsimidou M.Z. Further examination of antiradical properties of Crocus sativus stigmas extract rich in crocins. J Agric Food Chem 2009, 57:3080-3086.
52. Ordy J.M., Schjeide O.A. Univariate and multivariate models for evaluating long-term changes in neurobiological development, maturity and aging. Prog Brain Res 1973, 40:25-51.
53. Papandreou M.A., Dimakopoulou A., Linardaki Z.I., Cordopatis P., Klimis-Zacas D., Margarity M., et al. Effect of a polyphenol-rich wild blueberry extract on cognitive performance of mice, brain antioxidant markers and acetylcholinesterase activity. Behav Brain Res 2009, 198:352-358.
54. Papandreou M.A., Kanakis C.D., Polissiou M.G., Efthimiopoulos S., Cordopatis P., Margarity M., et al. Inhibitory activity on amyloid-beta aggregation and antioxidant properties of Crocus sativus stigmas extract and its crocin constituents. J Agric Food Chem 2006, 54:8762-8768.
55. Palozza P., Krinsky N.I. Antioxidant effects of carotenoids in vivo and in vitro, an overview. Meth Enzymol 1992, 213:403-420.
56. Perry E.K., Johnson M., Kerwin J.M., Piggott M.A., Court J.A., Shaw P.J., et al. Convergent cholinergic activities in aging and Alzheimer's disease. Neurobiol Aging 1992, 13:393-400.
57. Pitsikas N., Zisimopoulou S., Tarantilis P.A., Kanakis C.D., Polissiou M.G., Sakellaridis N. Effects of the active constituents of Crocus sativus L., crocins on recognition and spatial rat's memory. Behav Brain Res 2007, 183:141-146.
58. Pitsikas N., Sakellaridis N. Crocus sativus L. extracts antagonize memory impairments in different behavioural tasks in the rat. Behav Brain Res 2006, 173:112-115.
59. Plumb J.A., Milroy R., Kaye S.B. Effects of the pH dependence of 3-(4,5-dimethylthiazol-2-yl)-2,5-diphenyl-tetrazolium bromide-formazan absorption on chemosensitivity determined by a novel tetrazolium-based assay. Cancer Res 1989, 49:4435-4440.
60. Pradham S.N. Central neurotransmitters and aging. Life Sci 1980, 26:1643-1656.
61. Premkumar K., Abraham S.K., Santhiya S.T., Ramesh A. Protective effects of saffron (Crocus sativus Linn.) on genotoxins-induced oxidative stress in Swiss albino mice. Phytother Res 2003, 17:614-617.
62. Rama Sastry B.V., Janson V.E., Jaiswal N., Tayeb O.S. Changes in enzymes of the cholinergic system and acetylcholine release in the cerebra of aging male Fischer rats. Pharmacology 1983, 26:61-72.
63. Rieger F., Vigny M. Solubilization and physiochemical characterization of rat brain acetylcholinesterase: development and maturation of its molecular forms. J Neurochem 1976, 27:121-129.
64. Shukitt-Hale B., Lau F.C., Joseph J.A. Berry fruit supplementation and the aging brain. J Agric Food Chem 2008, 56:636-641.
65. Singh A., Naidu P.S., Kulkarni S.K. Reversal of aging and chronic ethanol-induced cognitive dysfunction by quercetin a bioflavonoid. Free Radic Res 2003, 37:1245-1252.
66. Soeda S., Ochiai T., Paopong L., Tanaka H., Shoyama Y., Shimeno H. Crocin suppresses tumor necrosis factor-alpha-induced cell death of neuronally differentiated PC-12 cells. Life Sci 2001, 69:2887-2898.
67. Srividhya R., Jyothilakshmi V., Arulmathi K., Senthilkumaran V., Kalaiselvi P. Attenuation of senescence-induced oxidative exacerbations in aged rat brain by (-)-epigallocatechin-3-gallate. Int J Devl Neurosci 2008, 26:217-223.
68. Strong R., Ann N.Y. Regionally selective manifestations of neostriatal aging. Acad Sci 1988, 515:161-177.
69. Sugiura M., Saito H., Abe K., Shoyama Y. Ethanol extract of Crocus sativus L. antagonizes the inhibitory action of ethanol on hippocampal long-term potentiation in vivo. Phytother Res 1995, 9:100-104.
70. Sugiura M., Shoyama Y., Saito H., Abe K. Crocin (crocetin di-gentiobiose ester) prevents the inhibitory effect of ethanol on long-term potentiation in the dentate gyrus in vivo. J Pharmacol Exp Ther 1994, 271:703-707.
71. Tarantilis P.A., Tsoupras G., Polissiou M. Determination of saffron (Crocus sativus L.) components in crude plant extract using high-performance liquid chromatography-UV-visible photodiode-array detection-mass spectrometry. J Chromatogr A 1995, 699:107-118.
72. Terry A.V., Buccafusco J.J. The cholinergic hypothesis of age and Alzheimer's disease-related cognitive deficits: recent challenges and their implications for novel drug development. J Pharmacol Exp Ther 2003, 306:821-827.
73. Trinh N.H., Hoblyn J., Mohanty S., Yaffe K. Efficacy of cholinesterase inhibitors in the treatment of neuropsychiatric symptoms and functional impairment in Alzheimer disease: a meta-analysis. JAMA 2003, 289:210-216.
74. Tseng T.H., Chu C.Y., Huang J.M., Shiow S.J., Wang C.J. Crocetin protects against oxidative damage in rat primary hepatocytes. Cancer Lett 1995, 97:61-67.
75. Vijayan V.K. Cholinergic enzymes in the cerebellum and the hippocampus of the senescent mouse. Exp Gerontol 1977, 12:7-11.
76. Wang H., Joseph J.A. Quantifying cellular oxidative stress by dichlorofluorescein assay using microplate reader. Free Radic Biol Med 1999, 27:612-616.
77. Xi L., Qian Z., Du P., Fu J. Pharmacokinetic properties of crocin (crocetin digentiobiose ester) following oral administration in rats. Phytomed 2007, 14:633-636.
78. Yufu F., Egashira T., Yamanaka Y. Age-related changes of cholinergic markers in the rat brain. Jpn J Pharmacol 1994, 66:247-255.
79. Zhang Y., Shoyama Y., Sugiura M., Saito H. Effects of Crocus sativus L. on the ethanol-induced impairment of passive avoidance performances in mice. Biol Pharm Bull 1994, 17:217-221.
80. Zheng Y.Q., Liu J.X., Wang J.N., Xu L. Effects of crocin on reperfusion-induced oxidative/nitrative injury to cerebral microvessels after global cerebral ischemia. Brain Res 2007, 1138:86-94.