Whole-food diet worsened cognitive dysfunction in an Alzheimer's disease mouse model

Neurobiology of Aging

Volumn 36, Issue 1, 2015, Pages 90-99

  Parrott, Matthew D ^a,b   Winocur, Gordon ^a,b,c   Bazinet, Richard P ^a   Ma, David W L ^d   Greenwood, Carol E ^a,b  

^a UNIVERSITY OF TORONTO   (Canada)

^b ROTMAN RESEARCH INSTITUTE   (Canada)

^c TRENT UNIVERSITY   (Canada)

^d UNIVERSITY OF GUELPH   (Canada)

Author keywords

Alzheimer; Cognitive function; Diet; Diet quality; Food; Mouse model; Neuroinflammation

Indexed keywords

AMYLOID BETA PROTEIN; INSULIN; TUMOR NECROSIS FACTOR ALPHA;

ALZHEIMER DISEASE; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BRAIN CORTEX; COGNITION; COGNITIVE DEFECT; CONTROLLED STUDY; DIET; FISH; FRUIT; GENE EXPRESSION; HIPPOCAMPUS; LEARNING; MOUSE; NERVOUS SYSTEM INFLAMMATION; NONHUMAN; SIGNAL TRANSDUCTION; SPATIAL MEMORY; TASK PERFORMANCE; TRANSGENIC MOUSE; VEGETABLE; WHOLE FOOD DIET; ADVERSE EFFECTS; ANIMAL; C3H MOUSE; C57BL MOUSE; DISEASE COURSE; DISEASE MODEL; METABOLISM; NEUROGENIC INFLAMMATION; OXIDATIVE STRESS; PSYCHOLOGY;

ALZHEIMER DISEASE; AMYLOID BETA-PEPTIDES; ANIMALS; COGNITION; DIET; DISEASE MODELS, ANIMAL; DISEASE PROGRESSION; HIPPOCAMPUS; MICE, INBRED C3H; MICE, INBRED C57BL; MICE, TRANSGENIC; NEUROGENIC INFLAMMATION; OXIDATIVE STRESS; TUMOR NECROSIS FACTOR-ALPHA;

EID: 84920417413     PISSN: 01974580     EISSN: 15581497     Source Type: Journal    
DOI: 10.1016/j.neurobiolaging.2014.08.013     Document Type: Article

References (94)

1. Amtul Z., Keet M., Wang L., Merrifield P., Westaway D., Rozmahel R.F. DHA supplemented in peptamen diet offers no advantage in pathways to amyloidosis: is it time to evaluate composite lipid diet?. PLoS One 2011, 6:e24094.
2. Anantharaman M., Tangpong J., Keller J.N., Murphy M.P., Markesbery W.R., Kiningham K.K., St Clair D.K. Beta-amyloid mediated nitration of manganese superoxide dismutase: implication for oxidative stress in a APPNLH/NLH X PS-1P264L/P264L double knock-in mouse model of Alzheimer's disease. Am. J. Pathol. 2006, 168:1608-1618.
3. Arendash G.W., Jensen M.T., Salem N., Hussein N., Cracchiolo J., Dickson A., Leighty R., Potter H. Adiet high in omega-3 fatty acids does not improve or protect cognitive performance in Alzheimer's transgenic mice. Neuroscience 2007, 149:286-302.
4. Arsenault D., Julien C., Tremblay C., Calon F. DHA improves cognition and prevents dysfunction of entorhinal cortex neurons in 3xTg-AD mice. PLoS One 2011, 6:e17397.
5. Bomfim T.R., Forny-Germano L., Sathler L.B., Brito-Moreira J., Houzel J.C., Decker H., Silverman M.A., Kazi H., Melo H.M., McClean P.L., Holscher C., Arnold S.E., Talbot K., Klein W.L., Munoz D.P., Ferreira S.T., De Felice F.G. An anti-diabetes agent protects the mouse brain from defective insulin signaling caused by Alzheimer's disease-associated Aβ oligomers. J.Clin. Invest. 2012, 122:1339-1353.
6. Broersen L.M., Kuipers A.A., Balvers M., van Wijk N., Savelkoul P.J., de Wilde M.C., van der Beek E.M., Sijben J.W., Hageman R.J., Kamphuis P.J., Kiliaan A.J. Aspecific multi-nutrient diet reduces Alzheimer-like pathology in young adult AβPPswe/PS1dE9 mice. J.Alzheimers Dis. 2013, 33:177-190.
7. Calabrese V., Cornelius C., Dinkova-Kostova A.T., Iavicoli I., Di Paola R., Koverech A., Cuzzocrea S., Rizzarelli E., Calabrese E.J. Cellular stress responses, hormetic phytochemicals and vitagenes in aging and longevity. Biochim. Biophys. Acta 2012, 1822:753-783.
8. Calon F., Lim G.P., Yang F., Morihara T., Teter B., Ubeda O., Rostaing P., Triller A., Salem N., Ashe K.H., Frautschy S.A., Cole G.M. Docosahexaenoic acid protects from dendritic pathology in an Alzheimer's disease mouse model. Neuron 2004, 43:633-645.
9. Chakrabarty P., Herring A., Ceballos-Diaz C., Das P., Golde T.E. Hippocampal expression of murine TNFα results in attenuation of amyloid deposition invivo. Mol. Neurodegener. 2011, 6:16.
10. Chakrabarty P., Jansen-West K., Beccard A., Ceballos-Diaz C., Levites Y., Verbeeck C., Zubair A.C., Dickson D., Golde T.E., Das P. Massive gliosis induced by interleukin-6 suppresses Aβ deposition invivo: evidence against inflammation as a driving force for amyloid deposition. FASEB J. 2010, 24:548-559.
11. Chishti M.A., Yang D.S., Janus C., Phinney A.L., Horne P., Pearson J., Strome R., Zuker N., Loukides J., French J., Turner S., Lozza G., Grilli M., Kunicki S., Morissette C., Paquette J., Gervais F., Bergeron C., Fraser P.E., Carlson G.A., George-Hyslop P.S., Westaway D. Early-onset amyloid deposition and cognitive deficits in transgenic mice expressing a double mutant form of amyloid precursor protein 695. J.Biol. Chem. 2001, 276:21562-21570.
12. Chua L.M., Lim M.L., Chong P.R., Hu Z.P., Cheung N.S., Wong B.S. Impaired neuronal insulin signaling precedes Aβ42 accumulation in female AβPPsw/PS1δE9 mice. J.Alzheimers Dis. 2012, 29:783-791.
13. Commenges D., Scotet V., Renaud S., Jacqmin-Gadda H., Barberger-Gateau P., Dartigues J.F. Intake of flavonoids and risk of dementia. Eur. J. Epidemiol. 2000, 16:357-363.
14. Craft S., Cholerton B., Baker L.D. Insulin and Alzheimer's disease: untangling the web. J.Alzheimers Dis. 2013, 33(Suppl 1):S263-S275.
15. Cristalli D.O., Arnal N., Marra F.A., de Alaniz M.J., Marra C.A. Peripheral markers in neurodegenerative patients and their first-degree relatives. J.Neurol. Sci. 2012, 314:48-56.
16. Davinelli S., Sapere N., Zella D., Bracale R., Intrieri M., Scapagnini G. Pleiotropic protective effects of phytochemicals in Alzheimer's disease. Oxid. Med. Cell. Longev. 2012, 2012:386527.
17. de la Monte S.M. Contributions of brain insulin resistance and deficiency in amyloid-related neurodegeneration in Alzheimer's disease. Drugs 2012, 72:49-66.
18. Denner L.A., Rodriguez-Rivera J., Haidacher S.J., Jahrling J.B., Carmical J.R., Hernandez C.M., Zhao Y., Sadygov R.G., Starkey J.M., Spratt H., Luxon B.A., Wood T.G., Dineley K.T. Cognitive enhancement with rosiglitazone links the hippocampal PPARγ and ERK MAPK signaling pathways. J.Neurosci. 2012, 32:16725-16735.
19. Dergal J.M., Gold J.L., Laxer D.A., Lee M.S., Binns M.A., Lanctot K.L., Freedman M., Rochon P.A. Potential interactions between herbal medicines and conventional drug therapies used by older adults attending a memory clinic. Drugs Aging 2002, 19:879-886.
20. Devore E.E., Kang J.H., Breteler M.M., Grodstein F. Dietary intakes of berries and flavonoids in relation to cognitive decline. Ann. Neurol. 2012, 72:135-143.
21. Dudal S., Krzywkowski P., Paquette J., Morissette C., Lacombe D., Tremblay P., Gervais F. Inflammation occurs early during the Aβ deposition process in TgCRND8 mice. Neurobiol. Aging 2004, 25:861-871.
22. Egert S., Rimbach G. Which sources of flavonoids: complex diets or dietary supplements?. Adv. Nutr. 2011, 2:8-14.
23. Frautschy S.A., Cole G.M. Why pleiotropic interventions are needed for Alzheimer's disease. Mol. Neurobiol. 2010, 41:392-409.
24. Frautschy S.A., Hu W., Kim P., Miller S.A., Chu T., Harris-White M.E., Cole G.M. Phenolic anti-inflammatory antioxidant reversal of Aβ-induced cognitive deficits and neuropathology. Neurobiol. Aging 2001, 22:993-1005.
25. Freund-Levi Y., Eriksdotter-Jonhagen M., Cederholm T., Basun H., Faxen-Irving G., Garlind A., Vedin I., Vessby B., Wahlund L.O., Palmblad J. Omega-3 fatty acid treatment in 174 patients with mild to moderate Alzheimer disease: OmegAD study: a randomized double-blind trial. Arch. Neurol. 2006, 63:1402-1408.
26. Gabbita S.P., Srivastava M.K., Eslami P., Johnson M.F., Kobritz N.K., Tweedie D., Greig N.H., Zemlan F.P., Sharma S.P., Harris-White M.E. Early intervention with a small molecule inhibitor for tumor necrosis factor-α prevents cognitive deficits in a triple transgenic mouse model of Alzheimer's disease. J.Neuroinflammation 2012, 9:99.
27. Galasko D.R., Peskind E., Clark C.M., Quinn J.F., Ringman J.M., Jicha G.A., Cotman C., Cottrell B., Montine T.J., Thomas R.G., Aisen P. Antioxidants for Alzheimer disease: a randomized clinical trial with cerebrospinal fluid biomarker measures. Arch. Neurol. 2012, 69:836-841.
28. Garg S.K., Vitvitsky V., Albin R., Banerjee R. Astrocytic redox remodeling by amyloid beta peptide. Antioxid. Redox Signal 2011, 14:2385-2397.
29. Ghosh D., LeVault K.R., Barnett A.J., Brewer G.J. Areversible early oxidized redox state that precedes macromolecular ROS damage in aging nontransgenic and 3xTg-AD mouse neurons. J.Neurosci. 2012, 32:5821-5832.
30. Giovannini M.G., Cerbai F., Bellucci A., Melani C., Grossi C., Bartolozzi C., Nosi D., Casamenti F. Differential activation of mitogen-activated protein kinase signalling pathways in the hippocampus of CRND8 transgenic mouse, a model of Alzheimer's disease. Neuroscience 2008, 153:618-633.
31. Giunta B., Hou H., Zhu Y., Salemi J., Ruscin A., Shytle R.D., Tan J. Fish oil enhances anti-amyloidogenic properties of green tea EGCG in Tg2576 mice. Neurosci. Lett. 2010, 471:134-138.
32. Grimm M.O., Kuchenbecker J., Grosgen S., Burg V.K., Hundsdorfer B., Rothhaar T.L., Friess P., de Wilde M.C., Broersen L.M., Penke B., Peter M., Vigh L., Grimm H.S., Hartmann T. Docosahexaenoic acid reduces amyloid beta production via multiple pleiotropic mechanisms. J.Biol. Chem. 2011, 286:14028-14039.
33. Gu Y., Nieves J.W., Stern Y., Luchsinger J.A., Scarmeas N. Food combination and Alzheimer disease risk: a protective diet. Arch. Neurol. 2010, 67:699-706.
34. Hallock P., Thomas M.A. Integrating the Alzheimer's disease proteome and transcriptome: a comprehensive network model of a complex disease. OMICS 2012, 16:37-49.
35. Harrison F.E., Allard J., Bixler R., Usoh C., Li L., May J.M., McDonald M.P. Antioxidants and cognitive training interact to affect oxidative stress and memory in APP/PSEN1 mice. Nutr. Neurosci. 2009, 12:203-218.
36. Houtcooper W.C. Food habits of rodents in a cultivated ecosystem. J.Mammal. 1978, 59:427-430.
37. Joseph J.A., Denisova N.A., Arendash G., Gordon M., Diamond D., Shukitt-Hale B., Morgan D. Blueberry supplementation enhances signaling and prevents behavioral deficits in an Alzheimer disease model. Nutr. Neurosci. 2003, 6:153-162.
38. Joseph J.A., Shukitt-Hale B., Denisova N.A., Bielinski D., Martin A., McEwen J.J., Bickford P.C. Reversals of age-related declines in neuronal signal transduction, cognitive, and motor behavioral deficits with blueberry, spinach, or strawberry dietary supplementation. J.Neurosci. 1999, 19:8114-8121.
39. Kaltschmidt B., Uherek M., Volk B., Baeuerle P.A., Kaltschmidt C. Transcription factor NF-κB is activated in primary neurons by amyloid β peptides and in neurons surrounding early plaques from patients with Alzheimer disease. Proc. Natl. Acad. Sci. U.S.A 1997, 94:2642-2647.
40. Kashon M.L., Ross G.W., O'Callaghan J.P., Miller D.B., Petrovitch H., Burchfiel C.M., Sharp D.S., Markesbery W.R., Davis D.G., Hardman J., Nelson J., White L.R. Associations of cortical astrogliosis with cognitive performance and dementia status. J.Alzheimers Dis. 2004, 6:595-604.
41. Kesse-Guyot E., Fezeu L., Andreeva V.A., Touvier M., Scalbert A., Hercberg S., Galan P. Total and specific polyphenol intakes in midlife are associated with cognitive function measured 13 years later. J.Nutr. 2012, 142:76-83.
42. Khan T.K., Alkon D.L. An internally controlled peripheral biomarker for Alzheimer's disease: Erk1 and Erk2 responses to the inflammatory signal bradykinin. Proc. Natl. Acad. Sci. U.S.A 2006, 103:13203-13207.
43. Kharrazi H., Vaisi-Raygani A., Rahimi Z., Tavilani H., Aminian M., Pourmotabbed T. Association between enzymatic and non-enzymatic antioxidant defense mechanism with apolipoprotein E genotypes in Alzheimer disease. Clin. Biochem. 2008, 41:932-936.
44. Landry S.O. The Rodentia as omnivores. Q.Rev. Biol. 1970, 45:351-372.
45. Lee Y.J., Choi D.Y., Lee Y.K., Lee Y.M., Han S.B., Kim Y.H., Kim K.H., Nam S.Y., Lee B.J., Kang Y.W., Yun Y.W., Oh K.W., Hong J.T. 4-O-methylhonokiol prevents memory impairment in the Tg2576 transgenic mice model of Alzheimer's disease via regulation of β-secretase activity. J.Alzheimers Dis. 2012, 29:677-690.
46. Lee H.P., Pancholi N., Esposito L., Previll L.A., Wang X., Zhu X., Smith M.A., Lee M.G. Early induction of oxidative stress in mouse model of Alzheimer disease with reduced mitochondrial superoxide dismutase activity. PLoS One 2012, 7:e28033.
47. -δδCT method. Methods 2001, 25:402-408.
48. Ma Q.L., Yang F., Rosario E.R., Ubeda O.J., Beech W., Gant D.J., Chen P.P., Hudspeth B., Chen C., Zhao Y., Vinters H.V., Frautschy S.A., Cole G.M. β-amyloid oligomers induce phosphorylation of tau and inactivation of insulin receptor substrate via c-Jun N-terminal kinase signaling: suppression by omega-3 fatty acids and curcumin. J.Neurosci. 2009, 29:9078-9089.
49. Maesako M., Uemura K., Kuzuya A., Sasaki K., Asada M., Watanabe K., Ando K., Kubota M., Akiyama H., Takahashi R., Kihara T., Shimohama S., Kinoshita A. Gain of function by phosphorylation in presenilin 1-mediated regulation of insulin signaling. J.Neurochem. 2012, 121:964-973.
50. Mattson M.P. Hormesis defined. Ageing Res. Rev. 2008, 7:1-7.
51. Maurin H., Lechat B., Dewachter I., Ris L., Louis J.V., Borghgraef P., Devijver H., Jaworski T., Van Leuven F. Neurological characterization of mice deficient in GSK3α highlight pleiotropic physiological functions in cognition and pathological activity as tau kinase. Mol. Brain 2013, 6:27.
52. McDonald R., Ergis A.-M., Winocur G. Functional dissociation of brain regions in learning and memory. Memory: Systems, Process, or Function 1999, 66-104. Oxford University Press, Oxford. J. Foster, M. Jelcic (Eds.).
53. McLaurin J., Kierstead M.E., Brown M.E., Hawkes C.A., Lambermon M.H., Phinney A.L., Darabie A.A., Cousin J.E., French J.E., Lan M.F., Chen F., Wong S.S., Mount H.T., Fraser P.E., Westaway D., St George-Hyslop P. Cyclohexanehexol inhibitors of Aβ aggregation prevent and reverse Alzheimer phenotype in a mouse model. Nat. Med. 2006, 12:801-808.
54. Medeiros R., Prediger R.D., Passos G.F., Pandolfo P., Duarte F.S., Franco J.L., Dafre A.L., Di Giunta G., Figueiredo C.P., Takahasi R.N., Campos M.M., Calixto J.B. Connecting TNF-α signaling pathways to iNOS expression in a mouse model of Alzheimer's disease: relevance for the behavioral and synaptic deficits induced by amyloid β protein. J.Neurosci. 2007, 27:5394-5404.
55. Morris M.C. Nutritional determinants of cognitive aging and dementia. Proc. Nutr. Soc. 2012, 71:1-13.
56. Morris R. Developments of a water-maze procedure for studying spatial learning in the rat. J.Neurosci. Methods 1984, 11:47-60.
57. Moscovitch M., Winocur G. Frontal lobes, memory, & aging. Structure and Function of Human Prefrontal Cortex 1995, 119-150. New York Academy of Sciences, New York. J. Grafman, K. Holyak, F. Boller (Eds.).
58. Murakami K., Murata N., Ozawa Y., Kinoshita N., Irie K., Shirasawa T., Shimizu T. Vitamin C restores behavioral deficits and amyloid-β oligomerization without affecting plaque formation in a mouse model of Alzheimer's disease. J.Alzheimers Dis. 2011, 26:7-18.
59. Nelson T.J., Sun M.K., Hongpaisan J., Alkon D.L. Insulin, PKC signaling pathways and synaptic remodeling during memory storage and neuronal repair. Eur. J. Pharmacol. 2008, 585:76-87.
60. Orr S.K., Trepanier M.O., Bazinet R.P. n-3 Polyunsaturated fatty acids in animal models with neuroinflammation. Prostaglandins Leukot. Essent. Fatty Acids 2013, 88:97-103.
61. Puertas M.C., Martinez-Martos J.M., Cobo M.P., Carrera M.P., Mayas M.D., Ramirez-Exposito M.J. Plasma oxidative stress parameters in men and women with early stage Alzheimer type dementia. Exp. Gerontol. 2012, 47:625-630.
62. Quinn J.F., Bussiere J.R., Hammond R.S., Montine T.J., Henson E., Jones R.E., Stackman R.W. Chronic dietary alpha-lipoic acid reduces deficits in hippocampal memory of aged Tg2576 mice. Neurobiol. Aging 2007, 28:213-225.
63. Quinn J.F., Raman R., Thomas R.G., Yurko-Mauro K., Nelson E.B., Van Dyck C., Galvin J.E., Emond J., Jack C.R., Weiner M., Shinto L., Aisen P.S. Docosahexaenoic acid supplementation and cognitive decline in Alzheimer disease: a randomized trial. JAMA 2010, 304:1903-1911.
64. Reeves P.G., Nielsen F.H., Fahey G.C. AIN-93 purified diets for laboratory rodents: final report of the American Institute of Nutrition ad hoc writing committee on the reformulation of the AIN-76A rodent diet. J.Nutr. 1993, 123:1939-1951.
65. Reza-Lopez S.A., Anderson G.H., Szeto I.M., Taha A.Y., Ma D.W. High vitamin intake by Wistar rats during pregnancy alters tissue fatty acid concentration in the offspring fed an obesogenic diet. Metabolism 2009, 58:722-730.
66. Rezai-Zadeh K., Arendash G.W., Hou H., Fernandez F., Jensen M., Runfeldt M., Shytle R.D., Tan J. Green tea epigallocatechin-3-gallate (EGCG) reduces β-amyloid mediated cognitive impairment and modulates tau pathology in Alzheimer transgenic mice. Brain Res. 2008, 1214:177-187.
67. Rivera E.J., Goldin A., Fulmer N., Tavares R., Wands J.R., de la Monte S.M. Insulin and insulin-like growth factor expression and function deteriorate with progression of Alzheimer's disease: link to brain reductions in acetylcholine. J.Alzheimers Dis. 2005, 8:247-268.
68. Robinson C.A., Clark A.W., Parhad I.M., Fung T.S., Bou S.S. Gene expression in Alzheimer neocortex as a function of age and pathologic severity. Neurobiol. Aging 1994, 15:681-690.
69. Romberg C., Horner A.E., Bussey T.J., Saksida L.M. Atouch screen-automated cognitive test battery reveals impaired attention, memory abnormalities, and increased response inhibition in the TgCRND8 mouse model of Alzheimer's disease. Neurobiol. Aging 2013, 34:731-744.
70. Sano M., Ernesto C., Thomas R.G., Klauber M.R., Schafer K., Grundman M., Woodbury P., Growdon J., Cotman C.W., Pfeiffer E., Schneider L.S., Thal L.J. Acontrolled trial of selegiline, alpha-tocopherol, or both as treatment for Alzheimer's disease. The Alzheimer's Disease Cooperative Study. N.Engl. J. Med. 1997, 336:1216-1222.
71. Scarmeas N., Stern Y., Tang M.X., Mayeux R., Luchsinger J.A. Mediterranean diet and risk for Alzheimer's disease. Ann. Neurol. 2006, 59:912-921.
72. Schuessel K., Schafer S., Bayer T.A., Czech C., Pradier L., Muller-Spahn F., Muller W.E., Eckert A. Impaired Cu/Zn-SOD activity contributes to increased oxidative damage in APP transgenic mice. Neurobiol. Dis. 2005, 18:89-99.
73. Shaftel S.S., Kyrkanides S., Olschowka J.A., Miller J.N., Johnson R.E., O'Banion M.K. Sustained hippocampal IL-1β overexpression mediates chronic neuroinflammation and ameliorates Alzheimer plaque pathology. J.Clin. Invest. 2007, 117:1595-1604.
74. Shahrokh L.E., Lukaszuk J.M., Prawitz A.D. Elderly herbal supplement users less satisfied with medical care than nonusers. J.Am. Diet. Assoc. 2005, 105:1138-1140.
75. Shi Q., Gibson G.E. Oxidative stress and transcriptional regulation in Alzheimer disease. Alzheimer Dis. Assoc. Disord. 2007, 21:276-291.
76. Shih P.H., Chan Y.C., Liao J.W., Wang M.F., Yen G.C. Antioxidant and cognitive promotion effects of anthocyanin-rich mulberry (Morus atropurpurea L.) on senescence-accelerated mice and prevention of Alzheimer's disease. J.Nutr. Biochem. 2010, 21:598-605.
77. Singh S.V., Singh K. Cancer chemoprevention with dietary isothiocyanates mature for clinical translational research. Carcinogenesis 2012, 33:1833-1842.
78. Sofic E., Sapcanin A., Tahirovic I., Gavrankapetanovic I., Jellinger K., Reynolds G.P., Tatschner T., Riederer P. Antioxidant capacity in postmortem brain tissues of Parkinson's and Alzheimer's diseases. J.Neural Transm. Suppl. 2006, 71:39-43.
79. Son T.G., Camandola S., Mattson M.P. Hormetic dietary phytochemicals. Neuromolecular Med. 2008, 10:236-246.
80. Spencer J.P., Abd El Mohsen M.M., Minihane A.M., Mathers J.C. Biomarkers of the intake of dietary polyphenols: strengths, limitations and application in nutrition research. Br. J. Nutr. 2008, 99:12-22.
81. Sweatt J.D. Mitogen-activated protein kinases in synaptic plasticity and memory. Curr. Opin. Neurobiol. 2004, 14:311-317.
82. Talbot K., Wang H.Y., Kazi H., Han L.Y., Bakshi K.P., Stucky A., Fuino R.L., Kawaguchi K.R., Samoyedny A.J., Wilson R.S., Arvanitakis Z., Schneider J.A., Wolf B.A., Bennett D.A., Trojanowski J.Q., Arnold S.E. Demonstrated brain insulin resistance in Alzheimer's disease patients is associated with IGF-1 resistance, IRS-1 dysregulation, and cognitive decline. J.Clin. Invest. 2012, 122:1316-1338.
83. Tann C.R., Singleton G.R., Coman B.J. Diet of the house mouse, Mus domesticus, in the Mallee wheatlands of North-western Victoria. Wildl. Res. 1993, 18:1-12.
84. Tarkowski E., Andreasen N., Tarkowski A., Blennow K. Intrathecal inflammation precedes development of Alzheimer's disease. J.Neurol. Neurosurg. Psychiatry 2003, 74:1200-1205.
85. Tweedie D., Ferguson R.A., Fishman K., Frankola K.A., Van Praag H., Holloway H.W., Luo W., Li Y., Caracciolo L., Russo I., Barlati S., Ray B., Lahiri D.K., Bosetti F., Greig N.H., Rosi S. Tumor necrosis factor-α synthesis inhibitor 3,6'-dithiothalidomide attenuates markers of inflammation, Alzheimer pathology and behavioral deficits in animal models of neuroinflammation and Alzheimer's disease. J.Neuroinflammation 2012, 9:106.
86. Valgimigli L., Iori R. Antioxidant and pro-oxidant capacities of ITCs. Environ. Mol. Mutagen. 2009, 50:222-237.
87. Veeranna, Kaji T., Boland B., Odrljin T., Mohan P., Basavarajappa B.S., Peterhoff C., Cataldo A., Rudnicki A., Amin N., Li B.S., Pant H.C., Hungund B.L., Arancio O., Nixon R.A. Calpain mediates calcium-induced activation of the erk1,2 MAPK pathway and cytoskeletal phosphorylation in neurons: relevance to Alzheimer's disease. Am. J. Pathol. 2004, 165:795-805.
88. Wang J., Ho L., Zhao W., Ono K., Rosensweig C., Chen L., Humala N., Teplow D.B., Pasinetti G.M. Grape-derived polyphenolics prevent Aβ oligomerization and attenuate cognitive deterioration in a mouse model of Alzheimer's disease. J.Neurosci. 2008, 28:6388-6392.
89. Wang X., Wu H., Chen H., Liu R., Liu J., Zhang T., Yu W., Hai C. Does insulin bolster antioxidant defenses via the extracellular signal-regulated kinases-protein kinase B-nuclear factor erythroid 2 p45-related factor 2 pathway?. Antioxid. Redox Signal 2012, 16:1061-1070.
90. Winocur G., Thompson C., Hakim A., Greenwood C. The effects of high- and low-risk environments on cognitive function in rats following 2-vessel occlusion of the carotid arteries: a behavioral study. Behav. Brain Res. 2013, 252:144-156.
91. Winocur G., Vardy J., Binns M.A., Kerr L., Tannock I. The effects of the anti-cancer drugs, methotrexate and 5-fluorouracil, on cognitive function in mice. Pharmacol. Biochem. Behav. 2006, 85:66-75.
92. Wu C.C., Hsu M.C., Hsieh C.W., Lin J.B., Lai P.H., Wung B.S. Upregulation of heme oxygenase-1 by Epigallocatechin-3-gallate via the phosphatidylinositol 3-kinase/Akt and ERK pathways. Life Sci. 2006, 78:2889-2897.
93. Yu R., Lei W., Mandlekar S., Weber M.J., Der C.J., Wu J., Kong A.N. Role of a mitogen-activated protein kinase pathway in the induction of phase II detoxifying enzymes by chemicals. J.Biol. Chem. 1999, 274:27545-27552.
94. Zhao Y., Calon F., Julien C., Winkler J.W., Petasis N.A., Lukiw W.J., Bazan N.G. Docosahexaenoic acid-derived neuroprotectin D1 induces neuronal survival via secretase- and PPARγ-mediated mechanisms in Alzheimer's disease models. PLoS One 2011, 6:e15816.