The senescence accelerated mouse (SAMP8) as a model for oxidative stress and Alzheimer's disease

Biochimica et Biophysica Acta - Molecular Basis of Disease

Volumn 1822, Issue 5, 2012, Pages 650-656

  Morley, John E ^a   Armbrecht, Harvey James ^a,b   Farr, Susan A ^a,b   Kumar, Vijaya B ^a,b  

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

^b VETERANS AFFAIRS MEDICAL CENTER   (United States)

Author keywords

Alzheimer's disease; Amyloid beta; Blood brain barrier; Oxidative damage; Senescence accelerated mouse (SAMP8)

Indexed keywords

AMYLOID BETA PROTEIN; MELATONIN; TAU PROTEIN;

AGING; ALZHEIMER DISEASE; AMYLOID PLAQUE; ANIMAL EXPERIMENT; ANIMAL MODEL; APOPTOSIS; ARTICLE; CONTROLLED STUDY; DENDRITIC SPINE; FEMALE; GLIOSIS; HORMESIS; MALE; MITOCHONDRION; MOUSE; NONHUMAN; OXIDATIVE STRESS; PATHOPHYSIOLOGY; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; PROTEOMICS; SENESCENCE; VASCULAR AMYLOIDOSIS;

AGING; ALZHEIMER DISEASE; AMYLOID BETA-PROTEIN PRECURSOR; ANIMALS; BRAIN; DISEASE MODELS, ANIMAL; HORMESIS; MELATONIN; MICE; MITOCHONDRIA; OXIDATIVE STRESS;

ANIMALIA;

EID: 84858157217     PISSN: 09254439     EISSN: 1879260X     Source Type: Journal    
DOI: 10.1016/j.bbadis.2011.11.015     Document Type: Article

References (110)

1. Morley J.E. Alzheimer's disease: future treatments. J. Am. Med. Dir. Assoc. 2011, 12:1-7.
2. Swerdlow R.H., Khan S.M. A "mitochondrial cascade hypothesis" for sporadic Alzheimer's disease. Med. Hypotheses 2004, 63:8-20.
3. Golde T.E., Dickson D., Hutton M. Filling the gaps in the abeta cascade hypothesis of Alzheimer's disease. Curr. Alzheimer Res. 2006, 3:421-430.
4. Moreira P.I., Santos M.S., Oliveira C.R., Shenk J.C., Nunomura A., Smith M.A., Zhu X., Perry G. Alzheimer disease and the role of free radicals in the pathogenesis of the disease. CNS Neurol. Disord. Drug Targets 2008, 7:3-10.
5. Coskun P.E., Beal M.F., Wallace D.C. Alzheimer's brains harbor somatic mtDNA control-region mutations that suppress mitochondrial transcription and replication. Proc. Natl. Acad. Sci. U. S. A. 2004, 101:10726-10731.
6. Cottrell D.A., Blakely E.L., Johnson M.A., Ince P.G., Turnbull D.M. Mitochondrial enzyme-deficient hippocampal neurons and choroidal cells in AD. Neurology 2001, 57:260-264.
7. Yao J., Du H., Yan S., Fang F., Wang C., Lue L.F., Guo L., Chen D., Stern D.M., Gunn Moore F.J., Xi Chen J., Arancio O., Yan S.S. Inhibition of amyloid-beta (Abeta) peptide-binding alcohol dehydrogenase-Abeta interaction reduces Abeta accumulatin and improves mitochondrial function in a mouse model of Alzheimer's disease. J. Neurosci. 2011, 31:2313-2320.
8. Du H., Guo L., Yan S., Sosunov A.A., Sosunov A.A., McKhann G.M., Yan S.S. Early deficits in synaptic mitochondria in an Alzheimer's disease mouse model. Proc. Natl. Acad. Sci. U. S. A. 2010, 107:18670-18675.
9. Hyun D.H., Mughal M.R., Yang H., Lee J.H., Ko E.J., Hunt N.D., de Cabo R., Mattson M.P. The plasma membrane redox system is impaired by amyloid β-peptide and in the hippocampus and cerebral cortex of 3xTgAD. Exp. Neurol. 2010, 225:423-429.
10. Robinson R.A., Lange M.B., Sultana R., Galvan V., Fombonne J., Gorostiza O., Zhang J., Sarrier G., Cai J., Pierce W.M., Bredesen D.E., Butterfield D.A. Differential expression and redox proteomics analyses of an Alzheimer disease transgenic mouse model: effects of the amyloid-β peptide of amyloid precursor protein (E). Neuroscience 2011, 177:207-222.
11. Hamel E., Nicolakakis N., Aboulkassim T., Ongali B., Tong X.K. Oxidative stress and cerebrovascular dysfunction in mouse models of Alzheimer's disease. Exp. Physiol. 2008, 93:116-120.
12. Takeda T., Josokawa M., Takeshita S., Irino M., Higuchi M., Matsushita T., Tomita Y., Yasushira K., Hamamoto H., Shimizu K., Ishii M., Yamamuro T. A new murine model of accelerated senescence. Mech. Ageing Dev. 1981, 17:183-194.
13. Nishiyama M., Takahashi H., Miyamato M. Senescence-accelerated mouse (SAMP8): an animal model for age-related circadian rhythm disorder. The SAM Model of Senescence 1994, 393-396. Elsevier Science BV, Amsterdam. T. Takeda (Ed.).
14. Miyamoto M. Characteristics of age-related behavioral changes in senescence-accelerated mouse SAMP8 and SAMP10. Exp. Gerontol. 1997, 32:139-148.
15. Powers D.C., Morley J.E., Flood J.F. Age-related changes in LFA-1 expression, cell adhesion, and PHA-induced proliferation by lymphocytes from senescence-accelerated mouse (SAM)-P/8 and AMP-R/1 substrains. Cell. Immunol. 1992, 141:444-456.
16. Morley J.E. The SAMP8 mouse: a model of Alzheimer disease?. Biogerontology 2002, 3:57-60.
17. Flood J.F., Farr S.A., Kaiser F.E., Morley J.E. Age-related impairment in learning but not memory in SAMP8 female mice. Pharmacol. Biochem. Behav. 1995, 50:661-664.
18. Xia C., Higuchi K., Shimizu M., Matsushita T., Kogishi K., Wang J., Chiba T., Festing M.F., Hosokawa M. Genetic typing of the senescence-accelerated mouse (SAM) strains with microsatellite markers. Mamm. Genome 1999, 10:235-238.
19. Yagi H., Katoh S., Akiguchi I., Takeda T. Age-related deterioration of ability of acquisition in memory and learning in senescence-accelerated mouse; SAM-P/8 as an animal model of disturbances in recent memory. Brain Res. 1988, 474:86-93.
20. Flood J.F., Morley J.E. Learning and memory in the SAMP8 mouse. Neurosci. Biobehav. Rev. 1998, 22:1-20.
21. Miyamoto M., Kiyota Y., Nishiyama M., Nagaoka A. Senescence-accelerated mouse (SAM): age-related reduced anxiety-like behavior in the SAM-P/8 strain. Physiol. Behav. 1994, 51:979-985.
22. Flood J.F., Morley J.E. Age-related changes in footshock avoidance acquisition and retention in senescence accelerated mouse (SAM). Neurobiol. Aging 1993, 14:153-157.
23. Flood J.F., Morley J.E. Early onset of age-related impairment of aversive and appetitive learning in the SAM-P/8 mouse. J. Gerontol. 1994, 47:852-859.
24. Miyamoto M. Characteristics of memory and behavioral disorders in SAMP8 mice. The SAM Model of Senescence 1994, 61-66. Elsevier Science B.V, Amsterdam. T. Takeda (Ed.).
25. Chen G.H., Wang C., Yangchen H.Y., Liu R.Y., Zhou J.N. Age-related changes in anxiety are task-specific in the senescence-accelerated prone mouse 8. Physiol. Behav. 2007, 91:644-651.
26. Markowska A., Spangler E.L., Ingram D.K. Behavioral assessment senescence-accelerated mouse (SAMP8 and R1). Physiol. Behav. 1998, 64:15-26.
27. Flood J.F., Morley J.E., La Reginna M. Age-related changes in the pharmacological improvement of retention in senescence accelerated mouse (SAM). Neurobiol. Aging 1993, 14:159-166.
28. Flood J.F., Farr S.A., Uezu K., Morley J.E. Age-related changes in septal serotonergic, GABAergic and glutamatergic facilitation of retention in SAMP8 mice. Mech. Ageing Dev. 1998, 105:173-188.
29. Flood J.F., Harris F.J., Morley J.E. Age-related changes in hippocampal drug facilitation of memory processing in SAMP8 mice. Neurobiol. Aging 1996, 17:15-24.
30. Sugiyama H., Akiyama H., Akiguchi I., Kameyama M., Takeda T. Loss of dendritic spines in hippocampal CA1 pyramidal cells in senescence accelerated mouse (SAM)-a quantitative Golgi study. Clin. Neurol. 1987, 27:841-845.
31. Akiyama H., Kameyama M., Akiguchi I., Sugiyama H., Kawamata T., Fukuyama H., Kimura H., Matsushita M., Takeda T. Periodic acid-Schiff (PAS)-positive granular structures increase in the brain of senescence accelerated mouse (SAM). Acta Neuropathol. 1986, 72:124-129.
32. Garcia-Matas S., Gutierrez-Cuesta J., Coto-Montes A., Rubio-Acero R., Diez-Vives C., Camius A., Pallas M., Sanfeliu C., Critofol R. Dysfunction of astrocytes in senescence-accelerated mice SAMP8 reduces their neuroprotective capacity. Aging Cell 2008, 7:630-640.
33. Wu Y., Zhang A.Q., Yew D.T. Age related changes of various markers of astrocytes in senescence-accelerated mice hippocampus. Neurochem. Int. 2005, 46:565-574.
34. Jucker M., Walker L.C., Schwarb P., Hengemihle J., Kuo H., Snow A.D., Bamert F., Ingram D.K. Age-related deposition of glia-associated fibrillar material in brains of C57BL/6 mice. Neuroscience 1994, 60:875-889.
35. Flood J.F., Morley P.M., Morley J.E. Age-related changes in learning, memory, and lipofuscin as a function of the percentage of SAMP8 genes. Physiol. Behav. 1995, 58:819-822.
36. Takemura M., Nakamura S., Akiguchi I., Ueno M., Oka N., Ishikawa S., Shimada A., Kimura J., Takeda T. Beta/A4 protein-like immunoreactive granular structures in the brain of senescence-accelerated mouse. Am. J. Pathol. 1993, 142:1887-1897.
37. Fukunari A., Kato A., Sasaki Y., Yoshimoto T., Ishiura S., Suzuki K., Nakajima T. Colocalization of prolyl endopeptidase and amyloid β-peptide in brains of senescence-accelerated mouse. Neurosci. Lett. 1994, 176:201-204.
38. Morley J.E., Kumar V.B., Bernardo A.E., Farr S.A., Uezu K., Tamosa N., Flood J.F. Beta-amyloid precursor polypeptide in SAMP8 mice affects learning and memory. Peptides 2000, 21:1761-1767.
39. Manich G., Mercader C., Del Valle J., Duran-Vilaregut J., Camins A., Pallas M., Vilaplana J., Pelegri C. Characterization of amyloid-β granules in the hippocampus of SAMP8 mice. J. Alzheimers Dis. 2011, 25:535-546.
40. Canudas A.M., Gutierrez-Cuesta J., Rodriguez M.I., Acuna-Castroviejo D., Sureda F.X., Camins A., Pallas M. Hyperphosphorylation of microtubule-associated protein tau in senescence-accelerated mouse (SAM). Mech. Ageing Dev. 2005, 126:1300-1304.
41. Caballero B., Vega-Naredo I., Sierra V., Huidobro-Fernandez C., Soria-Valles C., De Gonzalo-Calvo D., Tolivia D., Gutierrez-Cuesta J., Pallas M., Camins A., Rodriguez-Colunga M.J., Coto-Montes A. Favorable effects of a prolonged treatment with melatonin on the level of oxidative damage and neurodegeneration in senescence-accelerated mice. J. Pineal. Res. 2008, 45:302-311.
42. Kumar V.B., Franko M., Banks W.A., Kasinadhuni P., Farr S.A., Vyas K., Choudhuri V., Morley J.E. Increase in presenilin 1 (PS1) levels in senescence-accelerated mice (SAMP8) may indirectly impair memory by affecting amyloid precursor protein (APP) processing. J. Exp. Biol. 2009, 212(Pt 4):494-498.
43. Butterfield D.A., Poon H.F. The senescence-accelerated prone mouse (SAMP8): a model of age-related cognitive decline with relevance to alterations of the gene expression and protein abnormalities in Alzheimer's disease. Exp. Gerontol. 2005, 40:774-783.
44. Strong R., Reddy V., Morley J.E. Cholinergic deficits in the septal-hippocampal pathway of the SAM-P/8 senescence accelerated mouse. Brain Res. 2003, 966:150-156.
45. Kitamura Y., Zhao X.H., Ohnuki T., Takei M., Nomura Y. Age-related changes in transmitter glutamate and NMDA receptor/channels in the brain of senescence-accelerated mouse. Neurosci. Lett. 1992, 137:169-172.
46. Nomura Y., Kitamura Y., Ohnuki T., Arima T., Yamanaka Y., Sasaki K., Oomura Y. Alterations in aceylcholine, NMDA, benzodiazepine receptors and protein kinase C in the brain of the senescence-accelerated mouse: an animal model useful for studies on cognitive enhancers. Behav. Brain Res. 1997, 83:51-55.
47. Ali A.K., Banks W.A., Kumar V.B., Shah Gn, Lynch J.L., Farr S.A., Fleegal-DeMotta M.A., Morley J.E. Nitric oxide activity and isoenzyme expression in the senescence-accelerated mouse p8 model of Alzheimer's disease: effects of anti-amyloid antibody and antisense treatments. J. Gerontol. A Biol. Sci. Med. Sci. 2009, 64:1025-1030.
48. Chu L.W., Tam S., Lee P.W., Wong R.L., Yik P.Y., Tsui W., Song Y., Cheung B.M., Morley J.E., Lam K.S. Bioavailable testosterone is associated with a reduced risk of amnestic mild cognitive impairment in older men. Clin. Endocrinol. 2008, 68:589-598.
49. Chu L.W., Tam S., Wong R.L., Yik P.Y., Song Y., Cheung B.M., Morley J.E., Lam K.S. Bioavailable testosterone predicts a lower risk of Alzheimer's disease in older men. J. Alzheimers Dis. Aug 6 2010, [Epub ahead of print].
50. Flood J.F., Farr S.A., Kaiser F.E., La Regina M., Morley J.E. Age-related decrease of plasma testosterone in SAMP8 mice: replacement improves age-related impairment of learning and memory. Physiol. Behavior 1995, 57:669-673.
51. Morley J.E., Farr S.A., Flood J.F. Antibody to amyloid beta protein alleviates impaired acquisition, retention, and memory processing in SAMP8 mice. Neurobiol. Learn Med. 2002, 78:125-138.
52. Banks W.A., Farr S.A., Morley J.E., Wolf K.M., Geylis V., Steinitz M. Anti-amyloid beta protein antibody passage across the blood-brain barrier in the SAMP8 mouse model of Alzheimer's disease: an age-related selective uptake with reversal of learning impairment. Exp. Neurol. 2007, 206:248-256.
53. Zhang Y., He J.S., Wang J., Bao F.X., Pang S.Y., Yin F., Hu H.G., Pong X.L., Sun W.M., Zheng Y.P., Hou L.L., Hong T. Administration of amyloid-β42 oligomer-specific monoclonal antibody improved memory performance in SAMP8 mice. J. Alzheimers Dis. 2011, 23:551-561.
54. Kumar V.B., Farr S.A., Flood J.F., Kamlesh V., Franko M., Banks W.A., Morley J.E. Site-directed antisense oligonucleotide decreases the expression of amyloid precursor protein and reverses deficits in learning and memory in aged SAMP8 mice. Peptides 2000, 21:1769-1775.
55. Banks W.A., Farr S.A., Butt W., Kumar V.B., Franko M.W., Morley J.E. Delivery across the blood-brain barrier of antisense directed against amyloid beta: reversal of learning and memory deficits in mice overexpressing amyloid precursor protein. J. Pharmacol. Exp. Ther. 2001, 297:1113-1121.
56. Banks W.A., Kimar V.B., Farr S.A., Nakaoke R., Robinson J.M., Morley J.E. Impairments in brain-to-blood transport of amyloid-β and reabsorption of cerebrospinal fluid in an animal model of Alzheimer's disease are reversed by antisense directed against amyloid-β protein precursor. J. Alzheimers Dis. 2011, 23:599-605.
57. Pickrell A.M., Moraes C.T. What role does mitochondrial stress play in neurodegenerative diseases?. Methods Mol. Biol. 2010, 648:63-78.
58. Rodolfo C., Ciccosanti F., Giacomo G.D., Piacentini M., Fimia G.M. Proteomic analysis of mitochondrial dysfunction in neurodegenerative diseases. Expert Rev. Proteomics 2010, 7:519-542.
59. Sultana R., Butterfield D.A. Oxidatively modified, mitochondria-relevant brain proteins in subjects with Alzheimer disease and mild cognitive impairment. J. Bioenerg. Biomembr. 2009, 41:441-446.
60. Palacios H.H., Yendluri B.B., Parvathaneni K., Shadlinski V.B., Obrenovich M.E., Leszek J., Gokhman D., Gasiorowski K., Bragin V., Aliev G. Mitochondrion-specific antioxidants as drug treatments for Alzheimer disease. CNS Neurol. Disord. Drug Targets 2011, 10:149-162.
61. Sultana R., Perluigi M., Butterfield D.A. Redox proteomics identification of oxidatively modified proteins in Alzheimer's disease brain and invivo and in vitro models of AD centered around Abeta (1-42). J. Chromatogr. B Analyt. Technol. Biomed. Life Sci. 2006, 833:3-11.
62. Butterfield D.A. Amyloid beta-peptide (1-42)-induced oxidative stress and neurotoxicity: implications for neurodegeneration in Alzheimer's disease brain. A review. Free. Radic. Res. 2002, 36:1307-1313.
63. Muller W.E., Eckert A., Kurz C., Eckert G.P., Leuner K. Mitochondrial dysfunction: common final pathway in brain aging and Alzheimer's disease-therapeutic aspects. Mol. Neurobiol. 2010, 41:159-171.
64. Pallas M., Camins A., Smith M.A., Perry G., Lee H.G., Casadesis G. From aging to Alzheimer's disease: unveiling "the switch" with the senescence-accelerated mouse model (SAMP8). J. Alzheimers Dis. 2008, 15:615-624.
65. Nomura Y., Wang B.X., Qi S.B., Namba T., Kaneko S. Biochemical changes related to aging in the senescence-accelerated mouse. Exp. Gerontol. 1989, 24:49-55.
66. Liu J., Mori A. Age-associated changes in superoxide dismutase activity, thriobarbituric acid reactivity and reduced glutathione level in the brain and liver in senescence accelerated mice (SAM): a comparison with DDY mice. Mech. Ageing Dev. 1993, 71:23-30.
67. Sato E., Oda N., Ozaki N., Hashimoto S., Kurokawa T., Ishibashi S. Early and transient increase in oxidative stress in the cerebral cortex of senescence-accelerated mouse. Mech. Ageing Dev. 1996, 86:105-114.
68. Sato E., Kurokawea T., Oda N., Ishibashi S. Early appearance of abnormality of microperoxisomal enzymes in the cerebral cortex of senescence-accelerated mouse. Mech. Ageing Dev. 1996, 92:175-184.
69. Kumar V.B., Franko M.W., Farr S.A., Armbrecht J.H., Morley J.E. Identification of age-dependent changes in expression of senescence-accelerated mouse (SAMP8) hippocampal proteins by expression array analysis. Biochem. Biophy. Res. Commun. 2000, 272:657-661.
70. Han S., Rudd J.A., Hu Z.Y., Zhang L., Yew D.T., Fang M. Analysis of neuronal nitric oxide synthase expression and increasing astrogliosis in the brain of senescence-accelerated-prone 8 mice. Int. J. Neurosci. 2010, 120:602-608.
71. Wu Y., Zhang A.Q., Yew D.T. Age related changes of various markers of astrocytes I senescence-accelerated mice hippocampus. Neurochem. Int. 2005, 46:565-574.
72. Nagele R.G., Wegiel J., Venkataraman V., Imaki H., Wang K.C., Wegiel J. Contribution of glial cells to the development of amyloid plaques in Alzheimer's disease. Neurobiol. Aging 2004, 25:663-674.
73. Farr S.A., Poon H.F., Dogrukol-Ak D., Drake J., Banks W.A., Eyerman E., Butterfield D.A., Morley J.E. The antioxidants alpha-lipoic acid and N-acetylcysteine reverse memory impairment and brain oxidative stress in aged SAMP8 mice. J. Neurochem. 2003, 84:1173-1183.
74. Butterfield D.A., Reed T., Sultana R. Roles of 3-nitrotyrosine- and 4-hydroxynonenal-modified brain proteins in the progression and pathogenesis of Alzheimer's disease. Free. Radic. Res. 2011, 45:59-72.
75. Poon H.F., Castegna A., Farr S.A., Thongboonkerd V., Lynnn B.C., Banks W.A., Morley J.E., Klein J.B., Butterfield D.A. Quantitative proteomics analysis of specific protein expression and oxidative modification in aged senescence-accelerated-prone 8 mice brain. Neuroscience 2004, 126:915-926.
76. Castegna A., Aksenov M., Thongboonkerd V., Klein J.B., Pierce W.M., Booze R., Markesbery W.R., Butterfield D.A. Proteomic identification of oxidatively modified proteins in Alzheimer's disease brain. Part II: dihydropyrimidinase-related protein 2, alpha-enolase and heat shock cognate 71. J. Neurochem. 2002, 82:1524-1532.
77. Butterfield D.A., Lange M.L. Multifunctional roles of enolase in Alzheimer's disease: beyond altered glucose metabolism. J. Neurochem. 2009, 111:915-933.
78. Poon H.F., Farr S.A., Thongboonkerd V., Lynn B.C., Banks W.A., Morley J.E., Klein J.B., Butterfield D.A. Proteomic analysis of specific brain proteins in aged SAMP8 mice treated with alpha-lipoic acid: implications for aging and age-related neurodegenerative disorders. Neurchem. Int. 2005, 46:159-168.
79. Nishiyama N., Zhou Y., Saito H. Ameliorative effects of chronic treatment using DX-9386, a traditional Chinese prescription, on learning performance and lipid peroxide content in senescence accelerated mouse. Biol. Pharm. Bull. 1994, 17:1481-1484.
80. Morley J.E., Farr S.A., Kumar V.B., Banks W.A. Alzheimer's disease through the eye of a mouse. Acceptance lecture for the 2001 Gayle A. Olson and Richard D. Olson prize. Peptides 2002, 23:589-599.
81. Hung M.C., Shibasaki K., Yoshida R., Sato M., Imaizumi K. Learning behaviour and cerebral protein kinase C, antioxidant status, lipid composition in senescence-accelerated mouse: influence of a phosphatidylcholine-vitamin B12 diet. Br. J. Nutr. 2001, 86:163-171.
82. Petursdottir A.L., Farr S.A., Morley J.E., Banks W.A., Skuladottir G.V. Effect of dietary n-3 polyunsaturated fatty acids on brain lipid fatty acid composition, learning ability, and memory of senescence-accelerated mouse. J. Gerontol. A Biol. Sci. Med. Sci. 2008, 63:1153-1160.
83. Petursdottir A.L., Farr S.A., Morley J.E., Banks W.A., Skuladottir G.V. Lipid peroxidation in brain during aging in the senescence-accelerated mouse (SAM). Neurobiol. Aging 2007, 28:1170-1178.
84. Butterfield D.A., Koppal T., Howard B., Subramaniam R., Hall N., Hensley K., Yatin S., Allen K., Aksenov M., Aksenova M., Carney J. 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. 1998, 854:448-462.
85. Choi J.H., Kim D. Effects of age and dietary restriction on lifespan and oxidative stress of SAMP8 mice with learning and memory impairments. J. Nutr. Health Aging 2000, 4:182-186.
86. Nishimura H., Higuchi O., Tateshita K., Tomobe K., Okuma Nomura Y. Antioxidative activity and ameliorative effects of memory impairment of sulfur-containing compounds in Allium species. Biofactors 2006, 26:135-146.
87. Chan Y.C., Hosoda K., Tsai C.J., Yamamoto S., Wang M.F. Favorable effects of tea on reducing the cognitive deficits and brain morphological changes in senescence-accelerated mice. J. Nutr. Sci. Vitaminol. (Tokyo) 2006, 52:266-273.
88. Gong Y., Liu L., Xie B., Liao Y., Yang E., Sun Z. Ameliorative effects of lotus seedpod proanthocyanidins on cognitive deficits and oxidative damage in senescence-accelerated mice. Behav. Brain Res. 2008, 194:100-107.
89. 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.
90. Farr S.A., Price T.O., Dominguez L.J., Motisi A., Saiano F., Niehoff M.L., Morley J.E., Banks W.A., Ercal N., Barbagolo M. Extra virgin olive oil improves learning and memory in SAMP8 mice. J Alzheimers Dis. 2012, 28:81-92.
91. He X.L., Zhou W.Q., Bi M.G., Du G.H. Neuroprotective effects of icariin on memory impairment and neurochemical deficits in senescence-accelerated mouse pron 8 (SAMP8) mice. Brain Res. 2010, 1334:73-83.
92. Acuna Castroviejo D., Lopez L.C., Escames G., Lopez A., Garcia J.A., Reiter R.J. Melatonin-mitochondria interplay in health and disease. Curr. Top. Med. Chem. 2011, 11:221-240.
93. Cuesta S., Kireev R., Forman K., Garcia C., Escames G., Ariznavarreta C., Vara E., Tresguerres J.A. Melatonin improves inflammation processes in liver of senescence-accelerated prone male mice (SAMP8). Exp. Gerontol. 2010, 45:950-956.
94. Carretero M., Escames G., Lopez L.C., Venegas C., Dayoub J.C., Garcia L., Acuna-Castroviego D. Long-term melatonin administration protects brain mitochondria from aging. J. Pineal. Res. 2009, 47:192-200.
95. Rodriguez M.I., Escames G., Lopez L.C., Lopez A., Garcia J.A., Ortiz F., Sanchez V., Romeu M., Acuna-Castroviejo O. Improved mitochondrial function and increased life span after chronic melatonin treatment in senescent prone mice. Exp. Gerontol. 2006, 43:749-756.
96. Caballero B., Vega-Naredo I., Sierra V., Huidobro-Fernandez C., Soria-Valles C., DeGonzalo-Calvo D., Tolivia D., Gutierrez-Cuesta J., Pallas M., Camins A., Rodriguez-Colunga M.J., Coto-Montes A. Favorable effects of a prolonged treatment with melatonin on the level of oxidative damage and neurodegeneration in senescence-accelerated mice. J. Pineal. Res. 2008, 45:302-311.
97. Okatani Y., Wakatsuki A., Reiter R.J., Miyahara Y. Melatonin reduces oxidative damage of neural lipids and proteins in senescence-accelerated mouse. Neurobiol. Aging 2002, 23:639-644.
98. Gutierrez-Cuesta J., Sureda F.X., Romeu M., Canudas A.M., Caballero B., coto-Montes A., Camius A., Pallas M. Chronic administration of melatonin reduces cerebral injury biomarkers in SAMP8. J. Pineal. Res. 2007, 42:394-402.
99. Cheng S., Ma C., Qu H., Fan W., Pang J., He H. Differential effects of melatonin on hippocampal neurodegeneration in different aged accelerated senescence prone mouse-8. Neuro. Endocrinol. Lett. 2008, 29:91-99.
100. Poon H.F., Joshi G., Sultana R., Farr S.A., Banks W.A., Morley I.E., Calabrese V., Butterfield D.A. Antisense directed at the Abeta region of APP decreases brain oxidative markers in aged senescence accelerated mice. Brain Res. 2004, 1018:86-96.
101. Poon H.F., Farr S.A., Banks W.A., Pierce W.M., Klein J.B., Morley J.E., Butterfield D.A. Proteomic identification of less oxidized brain proteins in aged senescence-accelerated mice following administration of antisense oligonuleotide directed at the Abeta region of amyloid precursor protein. Brain Res. Mol. Brain Res. 2005, 138:8-16.
102. Deane R., Ziokovic B.V. Role of the blood-brain barrier in the pathogenesis of Alzheimer's disease. Curr. Alzheimer Res. 2007, 4:191-197.
103. Owen J.B., Sultana R., Aluise C.D., Erickson M.A., Price T.O., Bu G., Banks W.A., Butterfield D.A. Oxidative modification to LDL receptor-related protein 1 in hippocampus from subjects with Alzheimer disease: implications for Aβ accumulation in AD brain. Free Radic. Biol. Med. 2010, 49:1798-1803.
104. Morley J.E., Farr S.A., Banks W.A., Johnson S.N., Yamada K.A., Xu L. A physiological role for amyloid-beta protein enhancement of learning and memory. J. Alzheimers Dis. 2010, 19:441-449.
105. Puzzo D., Privitera L., Fa' M., Staniszewski A., Hashimoto G., Aziz F., Sakurai M., Ribe E.M., Troy C.M., Mercken M., Jung S.S., Palmeri A., Arancio O. Endogenous amyloid-β is necessary for hippocampal synaptic plasticity and memory. Ann. Neurol. 2011, 69:819-830.
106. Puzzo D., Privitera L., Leznik E., Fa M., Staniszewski A., Palmeri A., Arancio O. Picomolar amyloid-beta positively modulates synaptic plasticity and memory in hippocampus. J. Neurosci. 2008, 28:14537-14545.
107. Baruch-Suchodolsky R., Fischer B. Abeta40, either soluble or aggregated, is a remarkably potent antioxidant in cell-free oxidative systems. Biochemistry 2009, 48:4354-4370.
108. Nair N.G., Perry G., Smith M.A., Reddy V.P. NMR studies of zinc, copper, and iron binding to histidine, the principal metal ion complexing site of amyloid-beta peptide. J. Alzheimers Dis. 2010, 20:57-66.
109. Atwood C.S., Obrenovich M.E., Liu T., Chan H., Perry G., Smith M.A., Martins R.N. Amyloid-beta: a chameleon walking in two worlds: a review of the trophic and toxic properties of amyloid-beta. Brain Res. Brain Res. Rev. 2003, 43:1-16.
110. Friedlich A.L., Butcher L.L. Involvement of free oxygen radicals in beta-amyloidosis: an hypothesis. Neurobiol. Aging 1994, 15:443-455.