A canine model of human aging and Alzheimer's disease

Biochimica et Biophysica Acta - Molecular Basis of Disease

Volumn 1832, Issue 9, 2013, Pages 1384-1389

  Head, Elizabeth ^a  

^a UNIVERSITY OF KENTUCKY   (United States)

Author keywords

Beagle; Beta amyloid; Cognition; Mild cognitive impairment; Oxidative damage

Indexed keywords

AMYLOID BETA PROTEIN; HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE INHIBITOR;

AGING; ALZHEIMER DISEASE; ANIMAL MODEL; BRAIN BLOOD VESSEL; BRAIN FUNCTION; BRAIN MITOCHONDRION; CANINE MODEL; COGNITION; COGNITIVE DEFECT; DISORDERS OF MITOCHONDRIAL FUNCTIONS; HUMAN; LEARNING; MEMORY; MOLECULAR BIOLOGY; NERVE CELL LESION; NERVE DEGENERATION; NEUROBIOLOGY; NEUROFIBRILLARY TANGLE; NONHUMAN; PRIORITY JOURNAL; REVIEW; VASCULAR AMYLOIDOSIS; ANIMAL; DISEASE MODEL; DOG; PATHOLOGY; PHYSIOLOGY;

ANIMALIA; CANIS FAMILIARIS;

AGING; ALZHEIMER DISEASE; ANIMALS; DISEASE MODELS, ANIMAL; DOGS; HUMANS;

MLCS; MLOWN;

EID: 84881245274     PISSN: 09254439     EISSN: 1879260X     Source Type: Journal    
DOI: 10.1016/j.bbadis.2013.03.016     Document Type: Review

References (127)

1. Alberts A.W. Lovastatin and simvastatin - inhibitors of HMG CoA reductase and cholesterol biosynthesis. Cardiology 1990, 77:14-21.
2. Gerson R.J., MacDonald J.S., Alberts A.W., Kornbrust D.J., Majka J.A., Stubbs R.J., Bokelman D.L. Animal safety and toxicology of simvastatin and related hydroxy-methylglutaryl-coenzyme A reductase inhibitors. Am. J. Med. 1989, 87:28S-38S.
3. Axelsson E., Ratnakumar A., Arendt M.L., Maqbool K., Webster M.T., Perloski M., Liberg O., Arnemo J.M., Hedhammar A., Lindblad-Toh K. The genomic signature of dog domestication reveals adaptation to a starch-rich diet. Nature 2013, 495:360-364.
4. Greer K.A., Canterberry S.C., Murphy K.E. Statistical analysis regarding the effects of height and weight on life span of the domestic dog. Res. Vet. Sci. 2007, 82:208-214.
5. Galis F., Van der Sluijs I., Van Dooren T.J., Metz J.A., Nussbaumer M. Do large dogs die young?. J. Exp. Zool. B Mol. Dev. Evol. 2007, 308:119-126.
6. Patronek G.J., Waters D.J., Glickman L.T. Comparative longevity of pet dogs and humans: implications for gerontology research. J. Gerontol. A Biol. Sci. Med. Sci. 1997, 52:B171-B178.
7. Lowseth L.A., Gillett N.A., Gerlach R.F., Muggenburg B.A. The effects of aging on hematology and serum chemistry values in the beagle dog. Vet. Clin. Pathol. 1990, 19:13-19.
8. Cotman C.W., Head E. The canine (dog) model of human aging and disease: dietary, environmental and immunotherapy approaches. J. Alzheimers Dis. 2008, 15:685-707.
9. Mirra S.S. The CERAD neuropathology protocol and consensus recommendations for the postmortem diagnosis of Alzheimer's disease: a commentary. Neurobiol. Aging 1997, 18:S91-S94.
10. Selkoe D.J. Normal and abnormal biology of the beta-amyloid precursor protein. Annu. Rev. Neurosci. 1994, 17:489-517.
11. Walsh D.M., Klyubin I., Fadeeva J.V., Rowan M.J., Selkoe D.J. Amyloid-beta oligomers: their production, toxicity and therapeutic inhibition. Biochem. Soc. Trans. 2002, 30:552-557.
12. Lesne S., Koh M.T., Kotilinek L., Kayed R., Glabe C.G., Yang A., Gallagher M., Ashe K.H. A specific amyloid-beta protein assembly in the brain impairs memory. Nature 2006, 440:352-357.
13. Haass C., Selkoe D.J. Soluble protein oligomers in neurodegeneration: lessons from the Alzheimer's amyloid beta-peptide. Nat. Rev. Mol. Cell Biol. 2007, 8:101-112.
14. Iqbal K., Grundke-Iqbal I. Alzheimer neurofibrillary degeneration: significance, etiopathogenesis, therapeutics and prevention. J. Cell Mol. Med. 2008, 12:38-55.
15. Braak H., Braak E., Strothjohann M. Abnormally phosphorylated tau protein related to the formation of neurofibrillary tangels and neuropil threads in the cerebral cortex of sheep and goat. Neurosci. Lett. 1994, 171:1-4.
16. Nelson P.T., Greenberg S.G., Saper C.B. Neurofibrillary tangles in the cerebral cortex of sheep. Neurosci. Lett. 1994, 170:187-190.
17. Rosen R.F., Farberg A.S., Gearing M., Dooyema J., Long P.M., Anderson D.C., Davis-Turak J., Coppola G., Geschwind D.H., Pare J.F., Duong T.Q., Hopkins W.D., Preuss T.M., Walker L.C. Tauopathy with paired helical filaments in an aged chimpanzee. J. Comp. Neurol. 2008, 509:259-270.
18. Tapp P.D., Siwak C., Head E., Cotman C.W., Murphey H., Muggenburg B.A., Ikeda-Douglas C., Milgram N.W. Concept abstraction in the aging dog: development of a protocol using successive discrimination and size concept tasks. Behav. Brain Res. 2004, 153:199-210.
19. Siwak C.T., Tapp P.D., Head E., Zicker S.C., Murphey H.L., Muggenburg B.A., Ikeda-Douglas C.J., Cotman C.W., Milgram N.W. Chronic antioxidant and mitochondrial cofactor administration improves discrimination learning in aged but not young dogs. Prog. Neuropsychopharmacol. Biol. Psychiatry 2005, 29:461-469.
20. Milgram N.W., Zicker S.C., Head E., Muggenburg B.A., Murphey H., Ikeda-Douglas C., Cotman C.W. Dietary enrichment counteracts age-associated cognitive dysfunction in canines. Neurobiol. Aging 2002, 23:737-745.
21. Cotman C.W., Head E., Muggenburg B.A., Zicker S., Milgram N.W. Brain aging in the canine: a diet enriched in antioxidants reduces cognitive dysfunction. Neurobiol. Aging 2002, 23:809-818.
22. Head E., Callahan H., Muggenburg B.A., Cotman C.W., Milgram N.W. Visual-discrimination learning ability and beta-amyloid accumulation in the dog. Neurobiol. Aging 1998, 19:415-425.
23. Tapp P.D., Siwak C.T., Estrada J., Muggenburg B.A., Head E., Cotman C.W., Milgram N.W. Size and reversal learning in the beagle dog as a measure of executive function and inhibitory control in aging. Learn. Mem. 2003, 10:64-73.
24. Christie L.A., Studzinski C.M., Araujo J.A., Leung C.S., Ikeda-Douglas C.J., Head E., Cotman C.W., Milgram N.W. A comparison of egocentric and allocentric age-dependent spatial learning in the beagle dog. Prog. Neuropsychopharmacol. Biol. Psychiatry 2005, 29:361-369.
25. Studzinski C.M., Christie L.A., Araujo J.A., Burnham W.M., Head E., Cotman C.W., Milgram N.W. Visuospatial function in the beagle dog: an early marker of cognitive decline in a model of human aging and dementia. Neurobiol. Learn. Mem. 2006, 86:197-204.
26. Milgram N.W., Head E., Muggenburg B.A., Holowachuk D., Murphey H., Estrada J., Ikeda-Douglas C.J., Zicker S.C., Cotman C.W. Landmark discrimination learning in the dog: effects of age, an antioxidant fortified diet, and cognitive strategy. Neurosci. Biobehav. Rev. 2002, 26:679-695.
27. Milgram N.W., Adams B., Callahan H., Head E., Mackay W., Thirlwell C., Cotman C.W. Landmark discrimination learning in the dog. Learn. Mem. 1999, 6:54-61.
28. Milgram N.W., Head E., Weiner E., Thomas E. Cognitive functions and aging in the dog: acquisition of nonspatial visual tasks. Behav. Neurosci. 1994, 108:57-68.
29. Mishkin M., Delacour J. An analysis of short-term visual memory in the monkey. J. Exp. Psychol. Anim. Behav. Proc. 1975, 1:326-334.
30. Head E., Callahan H., Cummings B.J., Cotman C.W., Ruehl W.W., Muggenberg B.A., Milgram N.W. Open field activity and human interaction as a function of age and breed in dogs. Physiol. Behav. 1997, 62:963-971.
31. Head E., Mehta R., Hartley J., Kameka A.M., Cummings B.J., Cotman C.W., Ruehl W.W., Milgram N.W. Spatial learning and memory as a function of age in the dog. Behav. Neurosci. 1995, 109:851-858.
32. Chan A.D., Nippak P.M., Murphey H., Ikeda-Douglas C.J., Muggenburg B., Head E., Cotman C.W., Milgram N.W. Visuospatial impairments in aged canines (Canis familiaris): the role of cognitive-behavioral flexibility. Behav. Neurosci. 2002, 116:443-454.
33. Albert M.S., Funkenstein H.H. The effects of age: normal variation and its relation to disease. Disorders of the Nervous System: Clinical Neurology 1992, 598-611. Saunders Inc., Philadelphia. 2nd edition. A.K. Asburg, G.M. McKhanney, W.I. McDonald (Eds.).
34. Petersen R.C., Smith G.E., Waring S.C., Ivnik R.J., Kokmen E., Tangelos E.G. Aging, memory, and mild cognitive impairment. Int. Psychogeriatr. 1997, 9(Suppl. 1):65-69.
35. Petersen R.C., Smith G.E., Waring S.C., Ivnik R.J., Tangalos E.G., Kokmen E. Mild cognitive impairment: clinical characterization and outcome. Arch. Neurol. 1999, 56:303-308.
36. Adams B., Chan A., Callahan H., Milgram N.W. The canine as a model of human cognitive aging: recent developments. Prog. Neuropsychopharmacol. Biol. Psychiatry 2000, 24:675-692.
37. Head E., Milgram N.W., Cotman C.W. Neurobiological models of aging in the dog and other vertebrate species. Functional Neurobiology of Aging 2001, 457-468. Academic Press, San Diego. P. Hof, C. Mobbs (Ed.).
38. Baxter M.G., Gallagher M. Neurobiological substrates of behavioral decline: models and data analytic strategies for individual differences in aging. Neurobiol. Aging 1996, 491-495.
39. Markowska A.L., Stone W.S., Ingram D.K., Reynolds J., Gold P.E., Conti L.H., Pontecorvo M.J., Wenk G.L., Olton D.S. Individual differences in aging: behavioral and neurobiological correlates. Neurobiol. Aging 1989, 10:31-43.
40. Rapp P.R., Amaral D.G. Recognition memory deficits in a subpopulation of aged monkeys resemble the effects of medial temporal lobe damage. Neurobiol. Aging 1991, 12:481-486.
41. Rapp P.R. Neuropsychological analysis of learning and memory in aged nonhuman primates. Neurobiol. Aging 1993, 14:627-629.
42. Rapp P.R., Kansky M.T., Roberts J.A., Eichenbaum H. New directions for studying cognitive decline in old monkeys. Semin. Neurosci. 1994, 6:369-377.
43. Rowe J.W., Kahn R.L. Human aging: usual and successful. Science 1987, 237:143-149.
44. Su M.-Y., Head E., Brooks W.M., Wang Z., Muggenberg B.A., Adam G.E., Sutherland R.J., Cotman C.W., Nalcioglu O. MR imaging of anatomic and vascular characteristics in a canine model of human aging. Neurobiol. Aging 1998, 19:479-485.
45. Kimotsuki T., Nagaoka T., Yasuda M., Tamahara S., Matsuki N., Ono K. Changes of magnetic resonance imaging on the brain in beagle dogs with aging. J. Vet. Med. Sci. 2005, 67:961-967.
46. Gonzalez-Soriano J., Marin Garcia P., Contreras-Rodriguez J., Martinez-Sainz P., Rodriguez-Veiga E. Age-related changes in the ventricular system of the dog brain. Ann. Anat. 2001, 183:283-291.
47. Tapp P.D., Siwak C.T., Gao F.Q., Chiou J.Y., Black S.E., Head E., Muggenburg B.A., Cotman C.W., Milgram N.W., Su M.Y. Frontal lobe volume, function, and beta-amyloid pathology in a canine model of aging. J. Neurosci. 2004, 24:8205-8213.
48. Rofina J.E., van Ederen A.M., Toussaint M.J., Secreve M., van der Spek A., van der Meer I., Van Eerdenburg F.J., Gruys E. Cognitive disturbances in old dogs suffering from the canine counterpart of Alzheimer's disease. Brain Res. 2006, 1069:216-226.
49. Du A.T., Schuff N., Chao L.L., Kornak J., Ezekiel F., Jagust W.J., Kramer J.H., Reed B.R., Miller B.L., Norman D., Chui H.C., Weiner M.W. White matter lesions are associated with cortical atrophy more than entorhinal and hippocampal atrophy. Neurobiol. Aging 2005, 26:553-559.
50. Ezekiel F., Chao L., Kornak J., Du A.T., Cardenas V., Truran D., Jagust W., Chui H., Miller B., Yaffe K., Schuff N., Weiner M. Comparisons between global and focal brain atrophy rates in normal aging and Alzheimer disease: Boundary Shift Integral versus tracing of the entorhinal cortex and hippocampus. Alzheimer Dis. Assoc. Disord. 2004, 18:196-201.
51. Morita T., Mizutani Y., Sawada M., Shimada A. Immunohistochemical and ultrastructural findings related to the blood-brain barrier in the blood vessels of the cerebral white matter in aged dogs. J. Comp. Pathol. 2005, 133:14-22.
52. Tapp P.D., Head K., Head E., Milgram N.W., Muggenburg B.A., Su M.Y. Application of an automated voxel-based morphometry technique to assess regional gray and white matter brain atrophy in a canine model of aging. NeuroImage 2006, 29:234-244.
53. Jacqmot O., Van Thielen B., Fierens Y., Hammond M., Willekens I., Van Schuerbeek P., Verhelle F., Goossens P., De Ridder F., Clarys J.P., Vanbinst A., De Mey J. Diffusion tensor imaging of white matter tracts in the dog brain. Anat. Rec. 2013, 296:340-349.
54. Wu Y.C., Field A.S., Duncan I.D., Samsonov A.A., Kondo Y., Tudorascu D., Alexander A.L. High b-value and diffusion tensor imaging in a canine model of dysmyelination and brain maturation. NeuroImage 2011, 58:829-837.
55. Chambers J.K., Uchida K., Nakayama H. White matter myelin loss in the brains of aged dogs. Exp. Gerontol. 2012, 47:263-269.
56. Simic G., Kostovic I., Winblad B., Bogdanovic N. Volume and number of neurons of the human hippocampal formation in normal aging and Alzheimer's disease. J. Comp. Neurol. 1997, 379:482-494.
57. West M.J. Regionally specific loss of neurons in the aging human hippocampus. Neurobiol. Aging 1993, 14:287-293.
58. West M.J., Kawas C.H., Martin L.J., Troncoso J.C. The CA1 region of the human hippocampus is a hot spot in Alzheimer's disease. Ann. N. Y. Acad. Sci. 2000, 908:255-259.
59. Bobinski M., Wegiel J., Tarnawski M., Bobinski M., Reisberg B., de Leon M.J., Miller D.C., Wisniewski H.M. Relationships between regional neuronal loss and neurofibrillary changes in the hippocampal formation and duration and severity of Alzheimer disease. J. Neuropathol. Exp. Neurol. 1997, 56:414-420.
60. Siwak-Tapp C.T., Head E., Muggenburg B.A., Milgram N.W., Cotman C.W. Region specific neuron loss in the aged canine hippocampus is reduced by enrichment. Neurobiol. Aging 2008, 29:521-528.
61. Siwak-Tapp C.T., Head E., Muggenburg B.A., Milgram N.W., Cotman C.W. Neurogenesis decreases with age in the canine hippocampus and correlates with cognitive function. Neurobiol. Learn. Mem. 2007, 88:249-259.
62. Hwang I.K., Yoo K.Y., Li H., Choi J.H., Kwon Y.G., Ahn Y., Lee I.S., Won M.H. Differences in doublecortin immunoreactivity and protein levels in the hippocampal dentate gyrus between adult and aged dogs. Neurochem. Res. 2007, 32:1604-1609.
63. Pekcec A., Baumgartner W., Bankstahl J.P., Stein V.M., Potschka H. Effect of aging on neurogenesis in the canine brain. Aging Cell 2008, 7:368-374.
64. Swanson K.S., Vester B.M., Apanavicius C.J., Kirby N.A., Schook L.B. Implications of age and diet on canine cerebral cortex transcription. Neurobiol. Aging 2009, 30:1314-1326.
65. Johnstone E.M., Chaney M.O., Norris F.H., Pascual R., Little S.P. 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. 1991, 10:299-305.
66. Selkoe D.J., Bell D.S., Podlisny M.B., Price D.L., Cork L.C. Conservation of brain amyloid proteins in aged mammals and humans with Alzheimer's disease. Science 1987, 235:873-877.
67. Wisniewski H.M., Wegiel J., Morys J., Bancher C., Soltysiak Z., Kim K.S. Aged dogs: an animal model to study beta-protein amyloidogenesis. Alzheimer's disease. Epidemiology, Neuropathology, Neurochemistry and Clinics 1990, 151-167. Springer-Verlag, New York. P.R.K. Maurer, H. Beckman (Eds.).
68. Giaccone G., Verga L., Finazzi M., Pollo B., Tagliavini F., Frangione B., Bugiani O. Cerebral preamyloid deposits and congophilic angiopathy in aged dogs. Neurosci. Lett. 1990, 114:178-183.
69. Ishihara T., Gondo T., Takahashi M., Uchino F., Ikeda S., Allsop D., Imai K. Immunohistochemical and immunoelectron microscopial characterization of cerebrovascular and senile plaque amyloid in aged dogs' brains. Brain Res. 1991, 548:196-205.
70. Wisniewski H.M., Johnson A.B., Raine C.S., Kay W.J., Terry R.D. Senile plaques and cerebral amyloidosis in aged dogs. Lab. Investig. 1970, 23:287-296.
71. Wisniewski H.M. Wegiel, J., Morys, J., Bancher, C., Soltysiak, Z. and Kim, K.S., Aged dogs: an animal model to study beta-protein amyloidogenesis. Alzheimer's disease. Epidemiology, Neuropathology, Neurochemistry and Clinics 1990, 151-167. Springer-Verlag, New York. P.R.K. Maurer, H. Beckman (Eds.).
72. Head E., McCleary R., Hahn F.F., Milgram N.W., Cotman C.W. Region-specific age at onset of beta-amyloid in dogs. Neurobiol. Aging 2000, 21:89-96.
73. Braak H., Braak E. Neuropathological stageing of Alzheimer-related changes. Acta Neuropathol. 1991, 82:239-259.
74. Braak H., Braak E., Bohl J. Staging of Alzheimer-related cortical destruction. Rev. Clin. Neurosci. 1993, 33:403-408.
75. Thal D.R., Rub U., Orantes M., Braak H. Phases of A beta-deposition in the human brain and its relevance for the development of AD. Neurology 2002, 58:1791-1800.
76. Cummings B.J., Su J.H., Cotman C.W., White R., Russell M.J. Beta-amyloid accumulation in aged canine brain: a model of plaque formation in Alzheimer's disease. Neurobiol. Aging 1993, 14:547-560.
77. Colle M.-A., Hauw J.-J., Crespeau F., Uchiara T., Akiyama H., Checler F., Pageat P., Duykaerts C. Vascular and parenchymal Ab deposition in the aging dog: correlation with behavior. Neurobiol. Aging 2000, 21:695-704.
78. Cummings B.J., Head E., Afagh A.J., Milgram N.W., Cotman C.W. Beta-amyloid accumulation correlates with cognitive dysfunction in the aged canine. Neurobiol. Learn. Mem. 1996, 66:11-23.
79. Cummings B.J., Head E., Ruehl W.W., Milgram N.W., Cotman C.W. Beta-amyloid accumulation correlates with cognitive dysfunction in the aged canine. Neurobiol. Learn. Mem. 1996, 66:11-23.
80. Head E., Pop V., Sarsoza F., Kayed R., Beckett T.L., Studzinski C.M., Tomic J.L., Glabe C.G., Murphy M.P. Amyloid-beta peptide and oligomers in the brain and cerebrospinal fluid of aged canines. J. Alzheimers Dis. 2010, 20:637-646.
81. Kayed R., Head E., Thompson J.L., McIntire T.M., Milton S.C., Cotman C.W., Glabe C.G. Common structure of soluble amyloid oligomers implies common mechanism of pathogenesis. Science 2003, 300:486-489.
82. Attems J. Sporadic cerebral amyloid angiopathy: pathology, clinical implications, and possible pathomechanisms. Acta Neuropathol. 2005, 110:345-359.
83. Attems J., Jellinger K.A., Lintner F. Alzheimer's disease pathology influences severity and topographical distribution of cerebral amyloid angiopathy. Acta Neuropathol. 2005, 110:222-231.
84. Herzig M.C., Van Nostrand W.E., Jucker M. Mechanism of cerebral beta-amyloid angiopathy: murine and cellular models. Brain Pathol. 2006, 16:40-54.
85. Shimada A., Kuwamura M., Akawkura T., Umemura T., Takada K., Ohama E., Itakura C. Topographic relationship between senile plaques and cerebrovascular amyloidosis in the brain of aged dogs. J. Vet. Med. Sci. 1992, 54:137-144.
86. Uchida K., Tani Y., Uetsuka K., Nakayama H., Goto N. Immunohistochemical studies on canine cerebral amyloid angiopathy and senile plaques. J. Vet. Med. Sci. 1992, 54:659-667.
87. Uchida K., Nakayama H., Tateyama S., Goto N. Immunohistochemical analysis of constituents of senile plaques and cerebro-vascular amyloid in aged dogs. J. Vet. Med. Sci. 1992, 54:1023-1029.
88. Uchida K., Okuda R., Yamaguchi R., Tateyama S., Nakayama H., Goto N. Double-labeling immunohistochemical studies on canine senile plaques and cerebral amyloid angiopathy. J. Vet. Med. Sci. 1993, 55:637-642.
89. Uchida K., Kuroki K., Yoshino T., Yamaguchi R., Tateyama S. Immunohistochemical study of constituents other than beta-protein in canine senile plaques and cerebral amyloid angiopathy 1997, 93.
90. Uchida K., Miyauchi Y., Nakayama H., Goto N. Amyloid angiopathy with cerebral hemorrhage and senile plaque in aged dogs. Nippon. Juigaku. Zasshi. 1990, 52:605-611.
91. Uchida K., Nakayama H., Goto N. Pathological studies on cerebral amyloid angiopathy, senile plaques and amyloid deposition in visceral organs in aged dogs. J. Vet. Med. Sci. 1991, 53:1037-1042.
92. Yoshino T., Uchida K., Tateyama S., Yamaguchi R., Nakayama H., Goto N. A retrospective study of canine senile plaques and cerebral amyloid angiopathy. Vet. Pathol. 1996, 33:230-234.
93. Prior R., D'Urso D., Frank R., Prikulis I., Pavlakovic G. Loss of vessel wall viability in cerebral amyloid angiopathy. NeuroReport 1996, 7:562.
94. Deane R., Zlokovic B.V. Role of the blood-brain barrier in the pathogenesis of Alzheimer's disease. Curr. Alzheimer Res. 2007, 4:191-197.
95. Head E., Liu J., Hagen T.M., Muggenburg B.A., Milgram N.W., Ames B.N., Cotman C.W. Oxidative damage increases with age in a canine model of human brain aging. J. Neurochem. 2002, 82:375-381.
96. Skoumalova A., Rofina J., Schwippelova Z., Gruys E., Wilhelm J. The role of free radicals in canine counterpart of senile dementia of the Alzheimer type. Exp. Gerontol. 2003, 38:711-719.
97. Kiatipattanasakul W., Nakamura S., Kuroki K., Nakayama H., Doi K. Immunohistochemical detection of anti-oxidative stress enzymes in the dog brain. Neuropathology 1997, 17:307-312.
98. Opii W.O., Joshi G., Head E., Milgram N.W., Muggenburg B.A., Klein J.B., Pierce W.M., Cotman C.W., Butterfield D.A. 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 2008, 29:51-70.
99. Hwang I.K., Yoon Y.S., Yoo K.Y., Li H., Choi J.H., Kim D.W., Yi S.S., Seong J.K., Lee I.S., Won M.H. Differences in lipid peroxidation and Cu, Zn-superoxide dismutase in the hippocampal CA1 region between adult and aged dogs. J. Vet. Med. Sci. 2008, 70:273-277.
100. Papaioannou N., Tooten P.C.J., van Ederen A.M., Bohl J.R.E., Rofina J., Tsangaris T., Gruys E. Immunohistochemical investigation of the brain of aged dogs. I. Detection of neurofibrillary tangles and of 4-hydroxynonenal protein, an oxidative damage product, in senile plaques. Amyloid: J. Protein Folding Disord. 2001, 8:11-21.
101. Rofina J.E., Singh K., Skoumalova-Vesela A., van Ederen A.M., van Asten A.J., Wilhelm J., Gruys E. Histochemical accumulation of oxidative damage products is associated with Alzheimer-like pathology in the canine. Amyloid 2004, 11:90-100.
102. Barone E., Cenini G., Di Domenico F., Martin S., Sultana R., Mancuso C., Murphy M.P., Head E., Butterfield D.A. Long-term high-dose atorvastatin decreases brain oxidative and nitrosative stress in a preclinical model of Alzheimer disease: a novel mechanism of action. Pharmacol. Res. 2011, 63:172-180.
103. Shigenaga M.K., Hagen T.M., Ames B.N. Oxidative damage and mitochondrial decay in aging. Proc. Natl. Acad. Sci. U.S.A. 1994, 91:10771-10778.
104. Head E., Nukala V.N., Fenoglio K.A., Muggenburg B.A., Cotman C.W., Sullivan P.G. Effects of age, dietary, and behavioral enrichment on brain mitochondria in a canine model of human aging. Exp. Neurol. 2009, 220:171-176.
105. Milgram N.W., Head E., Zicker S.C., Ikeda-Douglas C.J., Murphey H., Muggenburg B., Siwak C., Tapp D., Cotman C.W. Learning ability in aged beagle dogs is preserved by behavioral enrichment and dietary fortification: a two-year longitudinal study. Neurobiol. Aging 2005, 26:77-90.
106. Pop V., Head E., Hill M.A., Gillen D., Berchtold N.C., Muggenburg B.A., Milgram N.W., Murphy M.P., Cotman C.W. Synergistic effects of long-term antioxidant diet and behavioral enrichment on beta-amyloid load and non-amyloidogenic processing in aged canines. J. Neurosci. 2010, 30:9831-9839.
107. Fahnestock M., Marchese M., Head E., Pop V., Michalski B., Milgram W.N., Cotman C.W. BDNF increases with behavioral enrichment and an antioxidant diet in the aged dog. Neurobiol. Aging 2012, 33:546-554.
108. Siwak-Tapp C.T., Head E., Muggenburg B.A., Milgram N.W., Cotman C.W. Region specific neuron loss in the aged canine hippocampus is reduced by enrichment. Neurobiol. Aging 2008, 29:39-50.
109. Cramer C., Haan M.N., Galea S., Langa K.M., Kalbfleisch J.D. Use of statins and incidence of dementia and cognitive impairment without dementia in a cohort study. Neurology 2008, 71:344-350.
110. Wolozin B., Kellman W., Ruosseau P., Celesia G.G., Siegel G. Decreased prevalence of Alzheimer disease associated with 3-hydroxy-3-methyglutaryl coenzyme A reductase inhibitors. Arch. Neurol. 2000, 57:1439-1443.
111. Wolozin B., Wang S.W., Li N.C., Lee A., Lee T.A., Kazis L.E. Simvastatin is associated with a reduced incidence of dementia and Parkinson's disease. BMC Med. 2007, 5:20.
112. Thelen K.M., Rentsch K.M., Gutteck U., Heverin M., Olin M., Andersson U., von Eckardstein A., Bjorkhem I., Lutjohann D. Brain cholesterol synthesis in mice is affected by high dose of simvastatin but not of pravastatin. J. Pharmacol. Exp. Ther. 2006, 316:1146-1152.
113. Murphy M.P., Morales J., Beckett T.L., Astarita G., Piomelli D., Weidner A., Studzinski C.M., Dowling A.L., Wang X., Levine H., Kryscio R.J., Lin Y., Barrett E., Head E. Changes in cognition and amyloid-beta processing with long term cholesterol reduction using atorvastatin in aged dogs. J. Alzheimers Dis. 2010, 22:135-150.
114. Schenk D., Barbour R., Dunn W., Gordon G., Grajeda H., Guido T., Hu K., Huang J., Johnson-Wood K., Khan K., Kholodenko D., Lee M., Liao Z., Lieberburg I., Motter R., Mutter L., Soriano F., Shopp G., Vasquez N., Vandevert C., Walker S., Wogulis M., Yednock T., Games D., Seubert P. Immunization with amyloid-beta attenuates Alzheimer-disease-like pathology in the PDAPP mouse. Nature 1999, 400:173-177.
115. Head E., Pop V., Vasilevko V., Hill M., Saing T., Sarsoza F., Nistor M., Christie L.A., Milton S., Glabe C., Barrett E., Cribbs D. A two-year study with fibrillar beta-amyloid (Abeta) immunization in aged canines: effects on cognitive function and brain Abeta. J. Neurosci. 2008, 28:3555-3566.
116. Gilman S., Koller M., Black R.S., Jenkins L., Griffith S.G., Fox N.C., Eisner L., Kirby L., Rovira M.B., Forette F., Orgogozo J.M. Clinical effects of Abeta immunization (AN1792) in patients with AD in an interrupted trial. Neurology 2005, 64:1553-1562.
117. Holmes C., Boche D., Wilkinson D., Yadegarfar G., Hopkins V., Bayer A., Jones R.W., Bullock R., Love S., Neal J.W., Zotova E., Nicoll J.A. Long-term effects of Abeta42 immunisation in Alzheimer's disease: follow-up of a randomised, placebo-controlled phase I trial. Lancet 2008, 372:216-223.
118. Martin S.B., Dowling A.L., Head E. Therapeutic interventions targeting Beta amyloid pathogenesis in an aging dog model. Curr. Neuropharmacol. 2011, 9:651-661.
119. Lai Z.C., Moss M.B., Killiany R.J., Rosene D.L., Herndon J.G. Executive system dysfunction in the aged monkey: spatial and object reversal learning. Neurobiol. Aging 1995, 16:947-954.
120. Rapp P.R. Visual discrimination and reversal learning in the aged monkey (Macaca mulatta). Behav. Neurosci. 1990, 104:876-884.
121. Cronin-Golomb A. Color vision, object recognition, and spatial localization in aging and Alzheimer's disease. Functional Neurobiology of Aging 2001, 517-529. Academic Press, San Diego. P.R. Hof, C.V. Mobbs (Eds.).
122. Boutet I., Milgram N.W., Freedman M. Cognitive decline and human (Homo sapiens) aging: an investigation using a comparative neuropsychological approach. J. Comp. Psychol. 2007, 121:270-281.
123. Freedman M., Oscar-Berman M. Spatial and visual learning deficits in Alzheimer's disease and Parkinson's disease. Brain Cognit. 1989, 11:114-126.
124. Emborg M.E., Ma S.Y., Mufson E.J., Levey A.I., Taylor M.D., Brown W.D., Holden J.E., Kordower J.H. Age-related declines in nigral neuronal function correlate with motor impairments in rhesus monkeys. J. Comp. Neurol. 1998, 401:253-265.
125. Kordower J.H., Liu Y.T., Winn S., Emerich D.F. Encapsulated PC12 cell transplants into hemiparkinsonian monkeys: a behavioral, neuroanatomical, and neurochemical analysis. Cell Transplant. 1995, 4:155-171.
126. Lezak M.D., Howieson D.B., Loring D.W. Neuropsychological Assessment 2004, Oxford University Press, New York. 4th ed.
127. Arnsten A.F.T., Goldman-Rakic P.S. Alpha 2-adrenergic mechanisms in prefrontal cortex associated with cognitive decline in aged nonhuman primates. Science 1985, 230:1273-1276.