A combination cocktail improves spatial attention in a canine model of human aging and Alzheimer's disease

Journal of Alzheimer's Disease

Volumn 32, Issue 4, 2012, Pages 1029-1042

  Head, Elizabeth ^a,b   Murphey, Heather L ^a   Dowling, Amy L S ^a   McCarty, Katie L ^a   Bethel, Samuel R ^a   Nitz, Jonathan A ^a   Pleiss, Melanie ^a   Vanrooyen, Jenna ^a   Grossheim, Mike ^a   Smiley, Jeffery R ^b   Murphy, M Paul ^a   Beckett, Tina L ^a   Pagani, Dieter ^c   Bresch, Frederick ^d   Hendrix, Curt ^e  

^a UNIVERSITY OF KENTUCKY   (United States)

^b UNIVERSITY OF KENTUCKY   (United States)

^c DP and Associates   (Canada)

^d Metacog Testing Systems   (Canada)

^e Akeso Health Sciences   (United States)

Author keywords

Alzheimer's disease; amyloid ; cognition; dog; inflammation; oxidative damage; spatial attention

Indexed keywords

ACETYLCYSTEINE; BLACK PEPPER EXTRACT; CURCUMIN; EPIGALLOCATECHINGALLATE; PIPERINE; THIOCTIC ACID; UNCLASSIFIED DRUG;

AGING; ALZHEIMER DISEASE; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CONTROLLED STUDY; DOG; DRINKING; FOOD COCKTAIL; LEARNING DISORDER; MEMORY DISORDER; NONHUMAN; PRIORITY JOURNAL; SPATIAL MEMORY; TEA;

EID: 84872332806     PISSN: 13872877     EISSN: 18758908     Source Type: Journal    
DOI: 10.3233/JAD-2012-120937     Document Type: Article

References (66)

1. Mirra SS, Heyman A, McKeel D, Sumi SM, Crain BJ, Brownlee LM, Vogel FS, Hughes JP, van Belle G, Berg L (1991) The Consortium to Establish a Registry for Alzheimer's Disease (CERAD). Part II. Standardization of the neuropathologic assessment of Alzheimer's disease. Neurology 41, 479-486.
2. Hardy JA, Higgins GA (1992) Alzheimer's disease: The amyloid cascade hypothesis. Science 256, 184-185.
3. Selkoe DJ (1996) Amyloid beta-protein and the genetics of Alzheimer's disease. J Biol Chem 271, 18295-18298.
4. Selkoe DJ, Schenk D (2003) Alzheimer's disease: Molecular understanding predicts amyloid-based therapeutics. Annu Rev Pharmacol Toxicol 43, 545-584.
5. Frautschy SA, Cole GM (2010)Whypleiotropic interventions are needed for Alzheimer's disease. Mol Neurobiol 41, 392-409.
6. Cai Z, Zhao B, Ratka A (2011) Oxidative stress and betaamyloid protein in Alzheimer's disease. Neuromolecular Med 13, 223-250.
7. Butterfield DA (1997) beta-Amyloid-associated free radical oxidative stress and neurotoxicity: Implications for Alzheimer's disease. Chem Res Toxicol 10, 495-506.
8. Butterfield DA, Bader Lange ML, Sultana R (2010) Involvements of the lipid peroxidation product, HNE, in the pathogenesis and progression of Alzheimer's disease. Biochim Biophys Acta 1801, 924-929.
9. Butterfield DA, Kanski J (2001) Brain protein oxidation in age-related neurodegenerative disorders that are associated with aggregated proteins. Mech Ageing Dev 122, 945-962.
10. Smith MA, Perry G, Richey PL, Sayre LM, Anderson VE, Beal MF, Kowall N (1996) Oxidative damage in Alzheimer's. Nature 382, 120-121.
11. Sultana R, Perluigi M, Butterfield DA (2006) Redox proteomics identification of oxidatively modified proteins in Alzheimer's disease brain and in vivo and in vitro models of AD centered around Abeta(1-42). J Chromatogr B Analyt Technol Biomed Life Sci 833, 3-11.
12. Sultana R, Perluigi M, Newman SF, Pierce WM, Cini C, Coccia R, Butterfield A (2010) Redox proteomic analysis of carbonylated brain proteins in mild cognitive impairment and early Alzheimer's disease. Antioxid Redox Signal 12, 327-336.
13. Nunomura A, Perry G, Pappolla MA, Wade R, Hirai K, Chiba S, Smith MA (1999) RNA oxidation is a prominent feature of vulnerable neurons in Alzheimer's disease. J Neurosci 19, 1959-1964.
14. Montine TJ, Neely MD, Quinn JF, Beal MF, Markesbery WR, Roberts LJ, Morrow JD (2002) Lipid peroxidation in aging brain and Alzheimer's disease. Free Radic Biol Med 33, 620-626.
15. Eikelenboom P, van Exel E, Hoozemans JJ, Veerhuis R, Rozemuller AJ, van Gool WA (2010) Neuroinflammation-an early event in both the history and pathogenesis of Alzheimer's disease. Neurodegener Dis 7, 38-41.
16. McGeer EG, McGeer PL (2010) Neuroinflammation in Alzheimer's disease and mild cognitive impairment: A field in its infancy. J Alzheimers Dis 19, 355-361.
17. Akiyama H, Barger S, Barnum S, Bradt B, Bauer J, Cole GM, Cooper NR, Eikelenboom P, Emmerling M, Fiebich BL, Finch CE, Frautschy S, Griffin WS, Hampel H, Hull M, Landreth G, Lue L, Mrak R, Mackenzie IR, McGeer PL, O'Banion MK, Pachter J, Pasinetti G, Plata-Salaman C, Rogers J, Rydel R, Shen Y, Streit W, Strohmeyer R, Tooyoma I, VanMuiswinkel FL, Veerhuis R, Walker D, Webster S, Wegrzyniak B, Wenk G, Wyss-Coray T (2000) Inflammation and Alzheimer's disease. Neurobiol Aging 21, 383-421.
18. Parachikova A, Green KN, Hendrix C, LaFerla FM (2010) Formulation of a medical food cocktail for Alzheimer's disease: Beneficial effects on cognition and neuropathology in a mouse model of the disease. PLoS ONE 5, e14015.
19. Walsh DM, Klyubin I, Fadeeva JV, Cullen WK, Anwyl R, Wolfe MS, Rowan MJ, Selkoe DJ (2002) Naturally secreted oligomers of amyloid beta protein potently inhibit hippocampal long-term potentiation in vivo. Nature 416, 535-539.
20. Cotman CW, HeadE(2008) The canine (dog) model of human aging and disease: Dietary, environmental and immunotherapy approaches. J Alzheimers Dis 15, 685-707.
21. Milgram NW, Head E, Weiner E, Thomas E (1994) Cognitive functions and aging in the dog: Acquisition of nonspatial visual tasks. Behav Neurosci 108, 57-68.
22. Head E, Milgram, NW, Cotman, CW (2001) Neurobiological models of aging in the dog and other vertebrate species. In Functional Neurobiology of Aging. Hof P, Mobbs C, ed. Academic Press, San Diego, pp. 457-468.
23. Studzinski CM, Christie LA, Araujo JA, Burnham WM, Head E, Cotman CW, Milgram NW (2006) Visuospatial function in the beagle dog: An early marker of cognitive decline in a model of human aging and dementia. Neurobiol Learn Mem 86, 197-204.
24. Wisniewski HM, Wegiel J, Morys J, Bancher C, Soltysiak Z, Kim KS (1990) Aged dogs: An animal model to study beta-protein amyloidogenesis. In Alzheimer's Disease. Epidemiology, Neuropathology, Neurochemistry and Clinics, Maurer K, Riederer P, Beckman H, eds. Springer-Verlag, New York, pp. 151-167.
25. Cummings BJ, Su JH, Cotman CW, White R, Russell MJ (1993) Beta-amyloid accumulation in aged canine brain: A model of plaque formation in Alzheimer's disease. Neurobiol Aging 14, 547-560.
26. Head E, McCleary R, Hahn FF, Milgram NW, Cotman CW (2000) Region-specific age at onset of beta-amyloid in dogs. Neurobiol Aging 21, 89-96.
27. Johnstone EM, Chaney MO, Norris FH, Pascual R, Little SP (1991) Conservation of the sequence of the Alzheimer's disease amyloid peptide in dog, polar bear and five other mammals by cross-species polymerase chain reaction analysis. Brain Res Mol Brain Res 10, 299-305.
28. Selkoe DJ, Bell DS, Podlisny MB, Price DL, Cork LC (1987) Conservation of brain amyloid proteins in aged mammals and humans with Alzheimer's disease. Science 235, 873-877.
29. Head E, Liu J, Hagen TM, Muggenburg BA, Milgram NW, Ames BN, Cotman CW (2002) Oxidative damage increases with age in a canine model of human brain aging. J Neurochem 82, 375-381.
30. Head E, Nukala VN, Fenoglio KA, Muggenburg BA, Cotman CW, Sullivan PG(2009) Effects of age, dietary, and behavioral enrichment on brain mitochondria in a canine model of human aging. Exp Neurol 220, 171-176.
31. Opii WO, Joshi G, Head E, Milgram NW, Muggenburg BA, Klein JB, Pierce WM, Cotman CW, Butterfield DA (2008) Proteomic identification of brain proteins in the canine model of human aging following a long-term treatment with antioxidants and a program of behavioral enrichment: Relevance to Alzheimer's disease. Neurobiol Aging 29, 51-70.
32. Cotman CW, Head E, Muggenburg BA, Zicker S, Milgram NW (2002) Brain aging in the canine: A diet enriched in antioxidants reduces cognitive dysfunction. Neurobiol Aging 23, 809-818.
33. Milgram NW, Head E, Zicker SC, Ikeda-Douglas C, Murphey H, Muggenberg BA, Siwak CT, Tapp PD, Lowry SR, Cotman CW (2004) Long-term treatment with antioxidants and a program of behavioral enrichment reduces age-dependent impairment in discrimination and reversal learning in beagle dogs. Exp Gerontol 39, 753-765.
34. Milgram NW, Head E, Muggenburg BA, Holowachuk D, Murphey H, Estrada J, Ikeda-Douglas CJ, Zicker SC, Cotman CW (2002) Landmark discrimination learning in the dog: Effects of age, an antioxidant fortified diet, and cognitive strategy. Neurosci Biobehav Rev 26, 679-695.
35. Milgram NW, Head E, Zicker SC, Ikeda-Douglas CJ, Murphey H, Muggenburg B, Siwak C, Tapp D, Cotman CW (2005) Learning ability in aged beagle dogs is preserved by behavioral enrichment and dietary fortification: A two-year longitudinal study. Neurobiol Aging 26, 77-90.
36. Pop V, Head E, Hill MA, Gillen D, Berchtold NC, Muggenburg BA, Milgram NW, Murphy MP, Cotman CW (2010) Synergistic effects of long-term antioxidant diet and behavioral enrichment on beta-amyloid load and nonamyloidogenic processing in aged canines. J Neurosci 30, 9831-9839.
37. Head E, Pop V, Vasilevko V, Hill M, Saing T, Sarsoza F, Nistor M, Christie LA, Milton S, Glabe C, Barrett E, Cribbs D(2008)Atwo-year study with fibrillar beta-amyloid (Abeta) immunization in aged canines: Effects on cognitive function and brain Abeta. J Neurosci 28, 3555-3566.
38. Head E, Mehta R, Hartley J, Kameka M, Cummings BJ, Cotman CW, Ruehl WW, Milgram NW (1995) Spatial learning and memory as a function of age in the dog. Behav Neurosci 109, 851-858.
39. Chan AD, Nippak PM, Murphey H, Ikeda-Douglas CJ, Muggenburg B, Head E, Cotman CW, Milgram NW (2002) Visuospatial impairments in aged canines (Canis familiaris): The role of cognitive-behavioral flexibility. Behav Neurosci 116, 443-454.
40. Milgram NW, Adams B, Callahan H, Head E, Mackay W, Thirlwell C, Cotman CW (1999) Landmark discrimination learning in the dog. Learn Memory 6, 54-61.
41. Milgram NW, Zicker SC, Head E, Muggenburg BA, Murphey H, Ikeda-Douglas C, Cotman CW (2002) Dietary enrichment counteracts age-associated cognitive dysfunction in canines. Neurobiol Aging 23, 737-745.
42. Milgram NW, Head E, Zicker SC, Ikeda-Douglas CJ, Murphey H, Muggenburg B, Siwak C, Tapp D, Cotman CW (2005) Learning ability in aged beagle dogs is preserved by behavioral enrichment and dietary fortification: A two-year longitudinal study. Neurobiol Aging 26, 77-90.
43. Kitamoto T, Ogomori K, Tateishi J, Prusiner SB (1987) Formic acid pretreatment enhances immunostaining of cerebral and systemic amyloids. Lab Invest 57, 230-236.
44. Head E, Pop V, Sarsoza F, Kayed R, Beckett TL, Studzinski CM, Tomic JL, Glabe CG, MurphyMP (2010) Amyloid-beta peptide and oligomers in the brain and cerebrospinal fluid of aged canines. J Alzheimers Dis 20, 637-646.
45. Murphy MP, Morales J, Beckett TL, Astarita G, Piomelli D, Weidner A, Studzinski CM, Dowling AL, Wang X, Levine H 3rd, Kryscio RJ, Lin Y, Barrett E, Head E (2010) Changes in cognition and amyloid-beta processing with long term cholesterol reduction using atorvastatin in aged dogs. J Alzheimers Dis 22, 135-150.
46. Pohl W (1973) Dissociation of spatial discrimination deficits following frontal and parietal lesions in monkeys. J Comp Physiol Psychol 82, 227-239.
47. Fernandez JW, Rezai-Zadeh K, Obregon D, Tan J (2010) EGCG functions through estrogen receptor-mediated activation of ADAM10 in the promotion of non-amyloidogenic processing of APP. FEBS Lett 584, 4259-4267.
48. Lee JW, Lee YK, Ban JO, Ha TY, Yun YP, Han SB, Oh KW, Hong JT (2009) Green tea (-)-epigallocatechin-3-gallate inhibits beta-amyloid-induced cognitive dysfunction through modification of secretase activity via inhibition of ERK and NF-kappaB pathways in mice. J Nutr 139, 1987-1993.
49. Bieschke J, Russ J, Friedrich RP, Ehrnhoefer DE, Wobst H, Neugebauer K, Wanker EE (2010) EGCG remodels mature alpha-synuclein and amyloid-beta fibrils and reduces cellular toxicity. Proc Natl Acad Sci USA 107, 7710-7715.
50. Lim GP, Chu T, Beech W, Frautschy SA, Cole GM (2001) The curry spice curcumin reduces oxidative damage and amyloid pathology in an Alzheimer transgenic mouse. J Neurosci 21, 8370-8377.
51. Tei M, Uchida K, Mutsuga M, Chambers JK, Nakayama H (2012) The binding of curcumin to various types of canine amyloid proteins. J Vet Med Sci 74, 481-483.
52. Mutsuga M, Chambers JK, Uchida K, Tei M, Makibuchi T, Mizorogi T, Takashima A, Nakayama H (2012) Binding of curcumin to senile plaques and cerebral amyloid angiopathy in the aged brain of various animals and to neurofibrillary tangles in Alzheimer's brain. J Vet Med Sci 74, 51-57.
53. Garcia-Alloza M, Borrelli LA, Rozkalne A, Hyman BT, Bacskai BJ (2007) Curcumin labels amyloid pathology in vivo, disrupts existing plaques, and partially restores distorted neurites in an Alzheimer mouse model. J Neurochem 102, 1095-1104.
54. Yang F, Lim GP, Begum AN, Ubeda OJ, Simmons MR, Ambegaokar SS, Chen PP, Kayed R, Glabe CG, Frautschy SA, Cole GM (2005) Curcumin inhibits formation of amyloid beta oligomers and fibrils, binds plaques, and reduces amyloid in vivo. J Biol Chem 280, 5892-5901.
55. Zhang C, Browne A, Child D, Tanzi RE (2010) Curcumin decreases amyloid-beta peptide levels by attenuating the maturation of amyloid-beta precursor protein. J Biol Chem 285, 28472-28480.
56. Hou Y, White RG, Bobik M, Marks JS, Russell MJ (1997) Distribution of beta-amyloid in the canine brain. NeuroReport 8, 1009-1012.
57. Dragicevic N, Smith A, Lin X, Yuan F, Copes N, Delic V, Tan J, Cao C, Shytle RD, Bradshaw PC (2011) Green tea epigallocatechin-3-gallate (EGCG) and other flavonoids reduce Alzheimer's amyloid-induced mitochondrial dysfunction. J Alzheimers Dis 26, 507-521.
58. He Y, Cui J, Lee JC, Ding S, Chalimoniuk M, Simonyi A, Sun AY, Gu Z, Weisman GA, Wood WG, Sun GY (2011) Prolonged exposure of cortical neurons to oligomeric amyloid-beta impairs NMDA receptor function via NADPH oxidase-mediated ROS production: Protective effect of green tea (-)-epigallocatechin-3-gallate. ASN Neuro 3, e00050.
59. Wang HM, Zhao YX, Zhang S, Liu GD, Kang WY, Tang HD, Ding JQ, Chen SD (2010) PPARgamma agonist curcumin reduces the amyloid-beta-stimulated inflammatory responses in primary astrocytes. J Alzheimers Dis 20, 1189-1199.
60. Ma QL, Yang F, Rosario ER, Ubeda OJ, Beech W, Gant DJ, Chen PP, Hudspeth B, Chen C, Zhao Y, Vinters HV, Frautschy SA, Cole GM (2009) Beta-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 29, 9078-9089.
61. Shoba G, Joy D, Joseph T, Majeed M, Rajendran R, Srinivas PS (1998) Influence of piperine on the pharmacokinetics of curcumin in animals and human volunteers. Planta Med 64, 353-356.
62. Lambert JD, Hong J, Kim DH, Mishin VM, Yang CS (2004) Piperine enhances the bioavailability of the tea polyphenol (-)-epigallocatechin-3-gallate in mice. J Nutr 134, 1948-1952.
63. Vijayakumar RS, Surya D, Nalini N (2004) Antioxidant efficacy of black pepper (Piper nigrum L. ) and piperine in rats with high fat diet induced oxidative stress. Redox Rep 9, 105-110.
64. Chonpathompikunlert P, Wattanathorn J, Muchimapura S (2010) Piperine, the main alkaloid of Thai black pepper, protects against neurodegeneration and cognitive impairment in animal model of cognitive deficit like condition of Alzheimer's disease. Food Chem Toxicol 48, 798-802.
65. Adair JC, Knoefel JE, Morgan N (2001) Controlled trial of Nacetylcysteine for patients with probable Alzheimer's disease. Neurology 57, 1515-1517.
66. Kapetanovic IM, Crowell JA, Krishnaraj R, Zakharov A, Lindeblad M, LyubimovA(2009) Exposure and toxicity of green tea polyphenols in fasted and non-fasted dogs. Toxicology 260, 28-36.