Extra virgin olive oil improves learning and memory in SAMP8 mice

Journal of Alzheimer's Disease

Volumn 28, Issue 1, 2012, Pages 81-92

  Farr, Susan A ^a,b   Price, Tulin O ^b   Dominguez, Ligia J ^c   Motisi, Antonio ^c   Saiano, Filippo ^c   Niehoff, Michael L ^b   Morley, John E ^a,b   Banks, William A ^d,e   Ercal, Nuran ^f   Barbagallo, Mario ^c  

^a VETERANS AFFAIRS MEDICAL CENTER   (United States)

^b SAINT LOUIS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c UNIVERSITY OF PALERMO   (Italy)

^d VA PUGET SOUND HEALTH CARE SYSTEM   (United States)

^e UNIVERSITY OF WASHINGTON SCHOOL OF MEDICINE   (United States)

^f MISSOURI UNIVERSITY OF SCIENCE AND TECHNOLOGY   (United States)

Author keywords

Extra virgin olive oil; learning; memory; object recognition; oxidative stress; SAMP8; T maze

Indexed keywords

3 NITROTYROSINE; 4 HYDROXYNONEAL 3 NITROTYROSINE; AMYLOID BETA PROTEIN; COCONUT OIL; EXTRA VIRGIN OLIVE OIL; GLUTATHIONE; GLUTATHIONE REDUCTASE; MILK FAT; OLIVE OIL; POLYPHENOL; SUPEROXIDE DISMUTASE; UNCLASSIFIED DRUG;

AGING; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BODY WEIGHT; BRAIN DAMAGE; BUTTER; CONTROLLED STUDY; DRUG EFFECT; DRUG MECHANISM; ENZYME ACTIVITY; FOOD INTAKE; FOOTSHOCK; LEARNING DISORDER; MAZE TEST; MEMORY DISORDER; MOUSE; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; RECOGNITION;

EID: 84855815138     PISSN: 13872877     EISSN: 18758908     Source Type: Journal    
DOI: 10.3233/JAD-2011-110662     Document Type: Article

References (54)

1. Trichopoulou A, Critselis E (2004) Mediterranean diet and longevity. Eur J Cancer Prev 13, 453-456. (Pubitemid 39341194)
2. Perez-Lopez FR, Chedraui P, Haya J, Cuadros JL (2009) Effects of the Mediterranean diet on longevity and age-related morbid conditions. Maturitas 64, 67-79.
3. Guallar-Castillon P, Rodriguez-Artalejo F, Tormo MJ, Sanchez MJ, Rodriguez L, Quiros JR, Navarro C, Molina E, Martinez C, Marin P, Lopez-Garcia E, Larrãnaga N, Huerta JM, Dorronsoro M, Chirlaque MD, Buckland G, Barricarte A, Banegas JR, Arriola L, Ardanaz E, Gonźalez CA, Moreno-Iribas C (2010) Major dietary patterns and risk of coronary heart disease in middle-aged persons from a Mediterranean country: The EPIC-Spain cohort study. Nutr Metab Cardiovasc Dis, doi:10.1016/j.numecd.2010.06.004.
4. Lopez-Miranda J, Perez-Jimenez F, Ros E, De Caterina R, Badimon L, Covas MI, Escrich E, Ordovas JM, Soriguer F, Abia R, de la Lastra CA, Battino M, Corella D, Chamorro-Quiŕos J, Delgado-Lista J, Giugliano D, Esposito K, Estruch R, Fernandez-Real JM, Gaforio JJ, La Vecchia C, Lairon D, Ĺopez-Segura F, Mata P, Meńendez JA, Muriana FJ, Osada J, Panagiotakos DB, Paniagua JA, Ṕerez-Martinez P, Perona J, Peinado MA, Pineda-Priego M, Poulsen JE, Quiles JL, Pamirez-Tortosa MC, Puano J, Serra-Majem L, Soĺa R, Solanas M, Solfrizzi V, de la Torre-Fornell R, Trichopoulou A, Uceda M, Villalba-Montoro JM, Villar-Ortiz JR, Visioli R, Yiannakouris N (2010) Olive oil and health: Summary of the II international conference on olive oil and health consensus report, Jaen and Cordoba (Spain) 2008. Nutr Metab Cardiovasc Dis 20, 284-294.
5. Calabrese V, Cornelius C, Trovato A, Cavallaro M, Mancuso C, Di Rienzo L, Condorelli D, De Lorenzo A, Calabrese EJ (2010) The hormetic role of dietary antioxidants in free radical-related diseases. Curr Pharm Des 16, 877-883.
6. Chan YC, Hosoda K, Tsai CJ, Yamamoto S, Wang MF (2006) Favorable effects of tea on reducing the cognitive deficits and brain morphological changes in senescence-accelerated mice. J Nutr Sci Vitaminol 52, 266-273. (Pubitemid 44520055)
7. Papandreou MA, Dimakopoulou A, Linardaki ZI, Cordopatis P, Klimis-Zacas D, Margarity M, Lamari FN (2009) Effect of a polyphenol-rich wild blueberry extract on cognitive performance of mice, brain antioxidant markers and acetylcholinesterase activity. Behav Brain Res 198, 352-358.
8. Scarmeas N, Stern Y, Mayeux R, Manly JJ, Schupf N, Luchsinger JA (2009) Mediterranean diet and mild cognitive impairment. Arch Neurol 66, 216-225.
9. Feart C, Samieri C, RondeauV, Amieva H, Portet F, Dartigues JF, Scarmeas N, Barberger-Gateau P (2009) Adherence to a Mediterranean diet, cognitive decline, and risk of dementia. JAMA 302, 638-648.
10. Scarmeas N, Stern Y, Tang MX, Mayeux R, Luchsinger JA (2006) Mediterranean diet and risk for Alzheimers disease. Ann Neurol 59, 912-921. (Pubitemid 43830923)
11. Shukitt-Hale B, Cheng V, Joseph JA (2009) Effects of blackberries on motor and cognitive function in aged rats. Nutr Neurosci 12, 135-140.
12. Shih PH, Chan YC, Liao JW, Wang MF, Yen GC (2010) Antioxidant and cognitive promotion effects of anthocyanin-rich mulberry (Morus atropurpurea L) on senescence-accelerated mice and prevention of Alzheimers disease. J Nutr Biochem 21, 598-605.
13. Assuncao M, Santos-Marques MJ, Carvalho F, Lukoyanov NV, Andrade JP (2011) Chronic green tea consumption prevents age-related changes in rat hippocampal formation. Neurobiol Aging 32, 707-717.
14. PitozziV, Jacomelli M, Zaid M, Luceri C, Bigagli E, Lodovici M, Ghelardini C, Vivoli E, Norcini M, Gianfriddo M, Esposto S, Servili M, Morozzi G, Baldi E, Bucherelli C, Dolara P, Giovannelli L (2010) Effects of dietary extra-virgin olive oil on behaviour and brain biochemical parameters in ageing rats. Br J Nutr 103, 1674-1683.
15. Ho L, Chen LH, Wang J, ZhaoW, Talcott ST, Ono K, Teplow D, Humala N, Cheng A, Percival SS, Ferruzzi M, Janle E, Dickstein Dl (2009) Heterogeneity in red wine polyphenolic contents differentially influences Alzheimers disease-type neuropathology and cognitive deterioration. J Alzheimers Dis 16, 59-72.
16. Kumar VB, Farr SA, Flood JF, Kamlesh V, Franko M, BanksWA, Morley JE (2000) Site-directed antisense oligonucleotide decreases the expression of amyloid precursor protein and reverses deficits in learning and memory in aged SAMP8 mice. Peptides 21, 1769-1775. (Pubitemid 32058851)
17. Morley JE, Kumar VB, Bernardo AE, Farr SA, Uezu K, Tumosa N, Flood JF (2002) Beta-amyloid precursor polypeptide in SAMP8 mice affects learning and memory. Peptides 21, 1761-1767.
18. Morley JE, Farr SA, Flood JF (2002) Antibody to amyloid beta protein alleviates impaired acquisition, retention, and memory processing in SAMP8 mice. Neurobiol Learn Mem 78, 125-138. (Pubitemid 34713254)
19. Takeda T (2009) Senescence-accelerated mouse (SAM) with special references to neurodegeneration models, SAMP8 and SAMP10 mice. Neurochem Res 34, 639-659.
20. Pallas M, Camins A, Smith MA, Perry G, Lee HG, Casadesus G (2008) From aging to Alzheimers disease: Unveiling "the switch" with the senescence-accelerated mouse model (SAMP8). J Alzheimers Dis 15, 615-624.
21. Butterfield DA, Koppal T, Howard B, Subramaniam R, Hall N, Hensley K, Yatin S, Allen K, Aksenov M, Aksenova M et al. (1998) Structural and functional changes in proteins induced by free radical-mediated oxidative stress and protective action of the antioxidants N-tert-butyl-alpha-phenylnitrone and vitamin E. Ann N Y Acad Sci 854, 448-462. (Pubitemid 29022824)
22. Poon HF, Castegna A, Farr SA, Thongboonkerd V, Lynn BC, Banks WA, Morley JE, Klein JB, ButterfieldDA(2004) Quantitative proteomics analysis of specific protein expression and oxidative modification in aged senescence-accelerated- prone mice brain. Neuroscience 126, 915-926. (Pubitemid 38780896)
23. Poon HF, Farr SA, Thongboonkerd V, Lynn BC, Banks WA, Morley JE, Klein JB, Butterfield DA (2005) Proteomic analysis of specific brain proteins in aged SAMP8 mice treated with alpha-lipoic acid: Implications for aging and age-related neurodegenerative disorders. Neurochem Int 46, 159-168. (Pubitemid 41556623)
24. Farr SA, Poon HF, Dogrukol-Ak D, Drake J, Banks WA, Eyerman E, Butterfield DA, Morley JE (2003) The antioxidants alpha-lipoic acid and N-acetylcysteine reverse memory impairment and brain oxidative stress in aged SAMP8 mice. J Neurochem 84, 1173-1183. (Pubitemid 36330669)
25. Montedoro GF, Servili M, Baldioli M, Selvaggini R, Miniati E, Macchioni A (1993) Simple and hydrolyzable compounds in virgin olive oil. Spectroscopic characterizations of the secoiridoid derivatives. J Agric Food Chem 41, 2228-2234.
26. Beauchamp GK, Keast RS, Morel D, Lin J, Pika J, Han Q, Lee CH, Smith AB, Breslin PA(2005) Phytochemistry: Ibuprofenlike activity in extra-virgin olive oil. Nature 437, 45-46. (Pubitemid 41613421)
27. Andrewes P, Busch JL, de Joode T, Groenewegen A, Alexandre H (2003) Sensory properties of virgin olive oil polyphenols: Identification of deacetoxy-ligstroside aglycon as a key contributor to pungency. J Agric Food Chem 51, 1415-1420.
28. Morellò JR, Motilva MJ, Tovar MJ, Romero MP (2004) Changes in commercial virgin olive oil (cv Arbequina) during storage, with special emphasis on the phenolic fraction. Food Chem 85, 357-364.
29. Singleton VL, Orthofer R, Lamuela-Raventos RM (1999) Analysis of total phenols and other oxidation substrates and antioxidants by means of Folin-Ciocalteu reagent. Meth Enzymol 299, 152-178. (Pubitemid 28483890)
30. Hammond RS, Tull LE, Stackman RW (2004) On the delay-dependent involvement of the hippocampus in object recognition memory. Neurobiol Learn Mem 82, 26-34. (Pubitemid 38737427)
31. Ridnour LA, Winters RA, Ercal N, Spitz DR (1999) Measurement of glutathione, glutathione disulfide, and other thiols in mammalian cell tissue homogenates using high-performance liquid chromatography separation of N-(1-pyrenyl)maleimide derivatives. Methods Enzymol 299, 258-267. (Pubitemid 28483898)
32. Winters RA, Zukowski J, Ercal N, Matthews RH, Spitz DR (1995) Analysis of glutathione, glutathione disulfide, cysteine, homocysteine, and other biological thiols by highperformance liquid chromatography following derivatization by n-(1-pyrenyl)maleimide. Anal Biochem 227, 14-21.
33. Draper HH, Squires EJ, Mahmoodi H, Wu J, Agarwal S, Hadley M (1993) A comparative evaluation of thiobarbituric acid methods for the determination of malondialdehyde in biological materials. Free Radic Biol Med 15, 353-363. (Pubitemid 23283552)
34. McCord JM, Keele BB Jr, Fridovich I (1971) An enzymebased theory of obligate anaerobiosis: The physiological function of superoxide dismutase. Proc Natl Acad Sci U S A 68, 1024-1027.
35. BradfordMA(1976) Rapid and sensitive method for the quantitation of microgram quantities of protein utilizing of the principle of protein-dye binding. Anal Biochem 72, 248-256.
36. Banks WA, Kumar VB, Farr SA, Nakaoke R, Robinson SM, Morley JE (2011) Impairments in brain-to-blood transport of amyloid-β and reabsorption of cerebrospinal fluid in an animal model of Alzheimers disease are reversed by antisense directed against amyloid-β protein precursor. J Alzheimers Dis 23, 599-605.
37. Farr SA, Banks WA, Uezu K, Sano A, Gaskin FS, Morley JE (2003) Antibody to beta-amyloid protein increases acetylcholine in the hippocampus of 12 month SAMP8 male mice. Life Sci 73, 555-562. (Pubitemid 36589035)
38. Banks WA, Robinson SM, Verma S, Morley JE. Efflux of human and mouse amyloid beta proteins 1-40 and 1-42 from brain: Impairment in a mouse model of Alzheimers disease. Neuroscience 121, 487-492.
39. Martinez-Gonzalez MA, Bes-Rastrollo M, Serra-Majem L, Lairon D, Estruch R, Trichopoulou A. Mediterranean food pattern and the primary prevention of chronic disease: recent developments. Nutr Rev 67 (Suppl 1), S111-S116.
40. Imoberdorf R, Ruhlin M, Ballmer PE (2005) (Eating and drinking during aging) (2005) Ther Umsch 62, 847-851.
41. Scislowski V, Bauchart D, Gruffat D, Laplaud PM, Durand D (2005) Effect of dietary n-6 and n-3 polyunsaturated fatty acids on peroxidizability of lipoproteins in steers. Lipids 40, 1245-1256. (Pubitemid 43117849)
42. Visioli F, Galli C (2002) Biological properties of olive oil phytochemicals. Crit Rev Food Sci Nutr 42, 209-221.
43. Frankel EN (2011) Nutritional and biological properties of extra virgin olive oil. J Agric Food Chem 59, 785-792.
44. Servili M, Selvaggini R, Esposto S, Taticchi A, Montedoro G, Morozzi G (2004) Health and sensory properties of virgin olive oil hydrophilic phenols: Agronomic and technological aspects of production that affect their occurrence in the oil. J Chromatogr 1054, 113-127. (Pubitemid 39445815)
45. Assuncao M, Santos-Marques MJ, Carvalho F, Andrade JP (2010) Green tea averts age-dependent decline of hippocampal signaling systems related to antioxidant defenses and survival. Free Radic Biol Med 48, 831-838.
46. Huertas JR, Martinez-Velasco E, Ibanez S, Lopez-Frias M, Ochoa JJ, Quiles J, Parenti Castelli G, Mataix J, Lenaz G (1999) Virgin olive oil and coenzyme Q10 protect heart mitochondria from peroxidative damage during aging. Biofactors 9, 337-343. (Pubitemid 29289016)
47. Ono K, Yoshiike Y, Takashima A, Hasegawa K, Naiki H, Yamada M (2003) Potent anti-amyloidogenic and fibrildestabilizing effects of polyphenols in vitro: Implications for the prevention and therapeutics of Alzheimers disease. J Neurochem 87, 172-181. (Pubitemid 37210651)
48. Wang YJ, Thomas P, Zhong JH, Bi FF, Kosaraju S, Pollard A, Fenech M, Zhou XF (2009) Consumption of grape seed extract prevents amyloid-beta deposition and attenuates inflammation in brain of an Alzheimers disease mouse. Neurotox Res 15, 3-14.
49. Krikorian R, Shidler MD, Nash TA, Kalt W, Vinqvist-Tymchuk MR, Shukitt-Hale B, Joseph JA (2010) Blueberry supplementation improves memory in older adults. J Agric Food Chem 58, 3996-4000.
50. Li W, Sperry JB, Crowe A, Trojanowski JQ, Smith AB, 3rd, Lee VM (2009) Inhibition of tau fibrillization by oleocanthal via reaction with the amino groups of tau. J Neurochem 110, 1339-1351.
51. Pitt J, Roth W, Lacor P, Smith AB, 3rd, Blankenship M, Velasco P, De Felice F, Breslin P, Klein WL (2009) Alzheimers-associated Abeta oligomers show altered structure, immunoreactivity and synaptotoxicity with low doses of oleocanthal. Toxicol Appl Pharmacol 240, 189-197.
52. Jacomelli M, Pitozzi V, Zaid M, Larrosa M, Tonini G, Martini A, Urbani S, Taticchi A, Servili M, Dolara P, JacomelliM (2010) Dietary extra-virgin olive oil rich in phenolic antioxidants and the aging process: Long-term effects in the rat. J Nutr Biochem 21, 290-296.
53. Umezawa M, Higuchi K, Mori M, Matushita T, HosokawaM (2009) Effect of dietary unsaturated fatty acids on senile amyloidosis in senescence-accelerated mice. J Gerontol A Biol Sci Med Sci 64, 646-652.
54. Marina AM, Man YB, Nazimah SA, Amin I (2009) Antioxidant capacity and phenolic acids of virgin coconut oil. Int J Food Sci Nutr 60 (Suppl 2), 114-123.