Nonhuman primate models of alzheimer-like cerebral proteopathy

Current Pharmaceutical Design

Volumn 18, Issue 8, 2012, Pages 1159-1169

  Heuer, Eric ^a,c   Rosen, Rebecca F ^a   Cintron, Amarallys ^a   Walker, Lary C ^a,b  

^a EMORY UNIVERSITY   (United States)

^b EMORY UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c UNIVERSITY OF HAWAII AT HILO   (United States)

Author keywords

Aging; Alzheimer's disease; Amyloid; Cerebral amyloid angiopathy; Monkeys; Neurodegeneration; Senile plaques; Tauopathy

Indexed keywords

AMYLOID BETA PROTEIN; AMYLOID PRECURSOR PROTEIN; TAU PROTEIN;

AGING; ALZHEIMER DISEASE; ARTICLE; CEREBRAL BETA AMYLOID ANGIOPATHY; CEREBROVASCULAR DISEASE; COGNITIVE DEFECT; DISEASE PREDISPOSITION; NERVE DEGENERATION; NEUROFIBRILLARY TANGLE; NEUROPATHOLOGY; NONHUMAN; PHYLOGENY; PRIMATE; PRIORITY JOURNAL; SENILE PLAQUE;

AGING; ALZHEIMER DISEASE; AMYLOID BETA-PEPTIDES; ANIMALS; BEHAVIOR, ANIMAL; BRAIN; DISEASE MODELS, ANIMAL; HUMANS; PRIMATES; SPECIES SPECIFICITY; TAU PROTEINS;

EID: 84857126830     PISSN: 13816128     EISSN: 18734286     Source Type: Journal    
DOI: 10.2174/138161212799315885     Document Type: Article

References (149)

1. Carter MD, Simms GA, Weaver DF. The development of new therapeutics for Alzheimer's disease. Clin Pharmacol Ther 2010; 88: 475-86.
2. Holtzman DM, Morris JC, Goate AM. Alzheimer's disease: the challenge of the second century. Sci Transl Med 2011; 3: 77sr1.
3. Hauw JJ, Duyckaerts C. Alzheimer's Disease. Oxford University Press: New York 2001.
4. Alzheimer A. A characteristic disease of the cerebral cortex. Allegemeine Zeitschrift fur Psychiatrie und Psychisch-Gerichtliche Medizin 1907; 64: 146.
5. Querfurth HW, LaFerla FM. Alzheimer's disease. N Engl J Med 2010; 362: 329-44.
6. Bekris LM, Yu CE, Bird TD, Tsuang DW. Genetics of Alzheimer disease. J Geriatr Psychiatry Neurol 2010; 23: 213-27.
7. Bertram L, Lill CM, Tanzi RE. The genetics of Alzheimer disease: back to the future. Neuron 2010; 68: 270-81.
8. Selkoe DJ. Biology of β-Amyloid Precursor Protein and the Mechanism of Alzheimer Disease. In: Terry RD, Katzman R, Bick KL, Sisodia SS, eds., Alzheimer Disease. Lippincott Williams & Wilkins: Philadelphia, PA 1999; pp. 293-310.
9. Murphy MP, LeVine H, 3rd. Alzheimer's disease and the amyloidbeta peptide. J Alzheimers Dis 2010; 19: 311-23.
10. Nimmrich V, Ebert U. Is Alzheimer's disease a result of presynaptic failure? Synaptic dysfunctions induced by oligomeric betaamyloid. Rev Neurosci 2009; 20: 1-12.
11. Kawahara M. Neurotoxicity of beta-amyloid protein: oligomerization, channel formation, and calcium dyshomeostasis. Curr Pharm Des 2010; 16: 2779-89.
12. Jin M, Shepardson N, Yang T, Chen G, Walsh D, Selkoe DJ. Soluble amyloid {beta}-protein dimers isolated from Alzheimer cortex directly induce Tau hyperphosphorylation and neuritic degeneration. Proc Natl Acad Sci USA 2011; 108: 5819-24.
13. Goedert M, Klug A, Crowther RA. Tau protein, the paired helical filament and Alzheimer's disease. J Alzheimers Dis 2006; 9: 195-207.
14. Lee VM, Goedert M, Trojanowski JQ. Neurodegenerative tauopathies. Annu Rev Neurosci 2001; 24: 1121-59.
15. Crystal H, Dickson D, Fuld P, et al. Clinico-pathologic studies in dementia: nondemented subjects with pathologically confirmed Alzheimer's disease. Neurology 1988; 38: 1682-7.
16. Giannakopoulos P, Gold G, Kovari E, et al. Assessing the cognitive impact of Alzheimer disease pathology and vascular burden in the aging brain: the Geneva experience. Acta Neuropathol (Berl) 2007; 113: 1-12.
17. Wilcock GK, Esiri MM. Plaques, tangles and dementia. A quantitative study. J Neurol Sci 1982; 56: 343-56.
18. Hardy J, Selkoe DJ. The amyloid hypothesis of Alzheimer's disease: progress and problems on the road to therapeutics. Science 2002; 297: 353-6.
19. Bolmont T, Clavaguera F, Meyer-Luehmann M, et al. Induction of tau pathology by intracerebral infusion of amyloid-beta -containing brain extract and by amyloid-beta deposition in APP x Tau transgenic mice. Am J Pathol 2007; 171: 2012-20.
20. Clavaguera F, Bolmont T, Crowther RA, et al. Transmission and spreading of tauopathy in transgenic mouse brain. Nat Cell Biol 2009; 11: 909-13.
21. Gotz J, Chen F, van Dorpe J, Nitsch RM. Formation of neurofibrillary tangles in P301l tau transgenic mice induced by Abeta 42 fibrils. Science 2001; 293: 1491-5.
22. Oddo S, Caccamo A, Tseng B, et al. Blocking Abeta42 accumulation delays the onset and progression of tau pathology via the C terminus of heat shock protein70-interacting protein: a mechanistic link between Abeta and tau pathology. J Neurosci 2008; 28: 12163-75.
23. Walker LC, Callahan MJ, Bian F, et al. Exogenous induction of cerebral beta-amyloidosis in betaAPP-transgenic mice. Peptides 2002; 23: 1241-7.
24. Walker LC, LeVine H, 3rd. The cerebral proteopathies. Neurobiol Aging 2000; 21: 559-61.
25. Levine H, Walker LC. Models of Alzheimer's disease. P. Michael Conn, Ed., Academic Press, Elsevier, New York, pp. 121-134 2006.
26. Jucker M. The benefits and limitations of animal models for translational research in neurodegenerative diseases. Nat Med 2010; 16: 1210-4.
27. Chow VW, Mattson MP, Wong PC, Gleichmann M. An overview of APP processing enzymes and products. Neuromolecular Med 2010; 12: 1-12.
28. Fiala JC. Mechanisms of amyloid plaque pathogenesis. Acta Neuropathol 2007; 114: 551-71.
29. Walker LC, Rosen RF, Levine H, 3rd. Diversity of Abeta deposits in the aged brain: a window on molecular heterogeneity? Rom J Morphol Embryol 2008; 49: 5-11.
30. Sani S, Traul D, Klink A, et al. Distribution, progression and chemical composition of cortical amyloid-beta deposits in aged rhesus monkeys: similarities to the human. Acta Neuropathol 2003; 105: 145-56.
31. Walker LC, Kitt CA, Cork LC, et al. Multiple transmitter systems contribute neurites to individual senile plaques. J Neuropathol Exp Neurol 1988; 47: 138-44.
32. Benzing WC, Brady DR, Mufson EJ, Armstrong DM. Evidence that transmitter-containing dystrophic neurites precede those containing paired helical filaments within senile plaques in the entorhinal cortex of nondemented elderly and Alzheimer's disease patients. Brain Res 1993; 619: 55-68.
33. Westermark P, Benson MD, Buxbaum JN, et al. A primer of amyloid nomenclature. Amyloid 2007; 14: 179-83.
34. Chiti F, Dobson CM. Protein misfolding, functional amyloid, and human disease. Annu Rev Biochem 2006; 75: 333-66.
35. Fandrich M. On the structural definition of amyloid fibrils and other polypeptide aggregates. Cell Mol Life Sci 2007; 64: 2066-78.
36. Wisniewski HM, Ghetti B, Terry RD. Neuritic (senile) plaques and filamentous changes in aged rhesus monkeys. J Neuropathol Exp Neurol 1973; 32: 566-84.
37. Sakono M, Zako T. Amyloid oligomers: formation and toxicity of Abeta oligomers. FEBS J 2010; 277: 1348-58.
38. Levine H, 3rd, Walker LC. Molecular polymorphism of Abeta in Alzheimer's disease. Neurobiol Aging 2010; 31: 542-8.
39. Revesz T, Ghiso J, Lashley T, et al. Cerebral amyloid angiopathies: a pathologic, biochemical, and genetic view. J Neuropathol Exp Neurol 2003; 62: 885-98.
40. Revesz T, Holton JL, Lashley T, et al. Genetics and molecular pathogenesis of sporadic and hereditary cerebral amyloid angiopathies. Acta Neuropathol 2009; 118: 115-30.
41. Rensink AA, de Waal RM, Kremer B, Verbeek MM. Pathogenesis of cerebral amyloid angiopathy. Brain Res Brain Res Rev 2003; 43: 207-23.
42. Greenberg SM, Gurol ME, Rosand J, Smith EE. Amyloid angiopathy-related vascular cognitive impairment. Stroke 2004; 35: 2616-9.
43. Okamoto Y, Ihara M, Ito H, Yamamoto T, Tomimoto H, Takashima R. Cortical microinfarcts are related to cerebral amyloid angiopathy rather than to senile plaques or neurofibrillary tangles. Neuroscience Meeting Planner. San Diego, CA. Society for Neuroscience, Online. 2010; Program Number 56.2.
44. Ellis RJ, Olichney JM, Thal LJ, et al. Cerebral amyloid angiopathy in the brains of patients with Alzheimer's disease: the CERAD experience, Part XV. Neurology 1996; 46: 1592-6.
45. Vinters HV. Cerebral amyloid angiopathy. A critical review. Stroke 1987; 18: 311-24.
46. Preston SD, Steart PV, Wilkinson A, Nicoll JA, Weller RO. Capillary and arterial cerebral amyloid angiopathy in Alzheimer's disease: defining the perivascular route for the elimination of amyloid beta from the human brain. Neuropathol Appl Neurobiol 2003; 29: 106-17.
47. Attems J, Jellinger KA. Only cerebral capillary amyloid angiopathy correlates with Alzheimer pathology--a pilot study. Acta Neuropathol 2004; 107: 83-90.
48. Eurelings LS, Richard E, Carrano A, Eikelenboom P, van Gool WA, Rozemuller AJ. Dyshoric capillary cerebral amyloid angiopathy mimicking Creutzfeldt-Jakob disease. J Neurol Sci 2010; 295: 131-4.
49. Maccioni RB, Farias G, Morales I, Navarrete L. The revitalized tau hypothesis on Alzheimer's disease. Arch Med Res 2010; 41: 226-31.
50. Ballatore C, Lee VM, Trojanowski JQ. Tau-mediated neurodegeneration in Alzheimer's disease and related disorders. Nat Rev Neurosci 2007; 8: 663-72.
51. McKee AC, Cantu RC, Nowinski CJ, et al. Chronic traumatic encephalopathy in athletes: progressive tauopathy after repetitive head injury. J Neuropathol Exp Neurol 2009; 68: 709-35.
52. Ikonomovic MD, Uryu K, Abrahamson EE, Ciallella JR, Trojanowski JQ, Lee VM, Clark RS, Marion DW, Wisniewski SR, De-Kosky ST. Alzheimer's pathology in human temporal cortex surgically excised after severe brain injury. Exp Neurol 2004; 190: 192-203.
53. Gong CX, Grundke-Iqbal I, Iqbal K. Targeting tau protein in Alzheimer's disease. Drugs Aging 2010; 27: 351-65.
54. Ballatore C, Brunden KR, Trojanowski JQ, Lee VM, Smith AB, 3rd, Huryn D. Modulation of Protein-Protein Interactions as a Therapeutic Strategy for the Treatment of Neurodegenerative Tauopathies. Curr Top Med Chem 2011; 11: 317-30.
55. Daviglus ML, Bell CC, Berrettini W, et al. National Institutes of Health State-of-the-Science Conference statement: preventing alzheimer disease and cognitive decline. Ann Intern Med 2010; 153: 176-81.
56. Werner P, Korczyn AD. Mild cognitive impairment: conceptual, assessment, ethical, and social issues. Clin Interv Aging 2008; 3: 413-20.
57. Warsch JR, Wright CB. The aging mind: vascular health in normal cognitive aging. J Am Geriatr Soc 2010; 58 Suppl 2: S319-24.
58. Murayama S, Saito Y. Neuropathological diagnostic criteria for Alzheimer's disease. Neuropathology 2004; 24: 254-60.
59. Williams BA, Kay RF, Kirk EC. New perspectives on anthropoid origins. Proc Natl Acad Sci USA 2010; 107: 4797-804.
60. Wilkinson RD, Steiper ME, Soligo C, Martin RD, Yang Z, Tavare S. Dating primate divergences through an integrated analysis of palaeontological and molecular data. Syst Biol 2011; 60: 16-31.
61. Finch CE, Sapolsky RM. The evolution of Alzheimer disease, the reproductive schedule, and apoE isoforms. Neurobiol Aging 1999; 20: 407-28.
62. Pawlik M, Fuchs E, Walker LC, Levy E. Primate-like amyloid-beta sequence but no cerebral amyloidosis in aged tree shrews. Neurobiol Aging 1999; 20: 47-51.
63. Rosen RF, Walker LC, Levine H, 3rd. PIB binding in aged primate brain: enrichment of high-affinity sites in humans with Alzheimer's disease. Neurobiol Aging 2011; 32: 223-34.
64. Adroer R, Lopez-Acedo C, Oliva R. Conserved elements in the 5' regulatory region of the amyloid precursor protein gene in primates. Neurosci Lett 1997; 226: 203-6.
65. Gearing M, Rebeck GW, Hyman BT, Tigges J, Mirra SS. Neuropathology and apolipoprotein E profile of aged chimpanzees: implications for Alzheimer disease. Proc Natl Acad Sci USA 1994; 91: 9382-6.
66. Gearing M, Tigges J, Mori H, Mirra SS. A beta40 is a major form of beta-amyloid in nonhuman primates. Neurobiol Aging 1996; 17: 903-8.
67. Kimura N, Nakamura S, Goto N, et al. Senile plaques in an aged western lowland gorilla. Exp Anim 2001; 50: 77-81.
68. Gearing M, Tigges J, Mori H, Mirra SS. beta-Amyloid (A beta) deposition in the brains of aged orangutans. Neurobiol Aging 1997; 18: 139-46.
69. Selkoe DJ, Bell DS, Podlisny MB, Price DL, Cork LC. Conservation of brain amyloid proteins in aged mammals and humans with Alzheimer's disease. Science 1987; 235: 873-7.
70. Rosen RF, Farberg AS, Hof PR, et al. The hippocampus of aged chimpanzees: regional neuron numbers, regional proportions and amyloid and tau pathology. In Preperation.
71. Marquez M, Serafin A, Fernandez-Bellon H, et al. Neuropathologic findings in an aged albino gorilla. Vet Pathol 2008; 45: 531-7.
72. Holzer M, Craxton M, Jakes R, Arendt T, Goedert M. Tau gene (MAPT) sequence variation among primates. Gene 2004; 341: 313-22.
73. Rosen RF, Farberg AS, Gearing M, et al. Tauopathy with paired helical filaments in an aged chimpanzee. J Comp Neurol 2008; 509: 259-70.
74. Mishkin M. Effects of small frontal lesions on delayed alternation in monkeys. Journal of Neurophysiology 1957; 20: 615-22.
75. Riopelle AJ, Rogers CM. Age changes in chimpanzees. Academic Press: New York 1965.
76. Kuhar C. Factors Affecting Spatial Ability of Lowland Gorillas: Age, Gender and Experience. Georgia Institute of Technology: Atlanta, GA 2004.
77. Martin LJ, Sisodia SS, Koo EH, et al. Amyloid precursor protein in aged nonhuman primates. Proc Natl Acad Sci USA 1991; 88: 1461-5.
78. Martin LJ, Pardo CA, Cork LC, Price DL. Synaptic pathology and glial responses to neuronal injury precede the formation of senile plaques and amyloid deposits in the aging cerebral cortex. Am J Pathol 1994; 145: 1358-81.
79. Podlisny MB, Tolan DR, Selkoe DJ. Homology of the amyloid beta protein precursor in monkey and human supports a primate model for beta amyloidosis in Alzheimer's disease. Am J Pathol 1991; 138: 1423-35.
80. Fukumoto H, Rosene DL, Moss MB, Raju S, Hyman BT, Irizarry MC. β-Secretasee Activity Increases with Aging in Human, Monkey and Mouse Brain. American Journal of Pathology 2004; 164: 719-25.
81. Sankaranarayanan S, Holahan MA, Colussi D, et al. First demonstration of cerebrospinal fluid and plasma A beta lowering with oral administration of a beta-site amyloid precursor protein-cleaving enzyme 1 inhibitor in nonhuman primates. J Pharmacol Exp Ther 2009; 328: 131-40.
82. Struble RG, Price DL, Jr., Cork LC, Price DL. Senile plaques in cortex of aged normal monkeys. Brain Res 1985; 361: 267-75.
83. Uno H, Walker LC. The age of biosenescence and the incidence of cerebral beta-amyloidosis in aged captive rhesus monkeys. Ann N Y Acad Sci 1993; 695: 232-5.
84. Walker ML. Menopause in female rhesus monkeys. American Journal of Primatology 1995; 35: 59-71.
85. Walker ML, Herndon JG. Menopause in nonhuman primates? Biol Reprod 2008; 79: 398-406.
86. Correia SC, Santos RX, Cardoso S, et al. Effects of estrogen in the brain: is it a neuroprotective agent in Alzheimer's disease? Curr Aging Sci 2010; 3: 113-26.
87. Simpkins JW, Yi KD, Yang SH, Dykens JA. Mitochondrial mechanisms of estrogen neuroprotection. Biochim Biophys Acta 2010; 1800: 1113-20.
88. Heilbroner PL, Kemper TL. The cytoarchitectonic distribution of senile plaques in three aged monkeys. Acta Neuropathol 1990; 81: 60-5.
89. Mufson EJ, Benzing WC, Cole GM, et al. Apolipoprotein Eimmunoreactivity in aged rhesus monkey cortex: colocalization with amyloid plaques. Neurobiol Aging 1994; 15: 621-7.
90. Thal DR, Capetillo-Zarate E, Del Tredici K, et al. Sci Aging Knowledge Environ 2006; 6, re1.
91. Poduri A, Gearing M, Rebeck GW, Mirra SS, Tigges J, Hyman BT. Apolipoprotein E4 and beta amyloid in senile plaques and cerebral blood vessels of aged rhesus monkeys. Am J Pathol 1994; 144: 1183-7.
92. Cork LC, Masters C, Beyreuther K, Price DL. Development of senile plaques. Relationships of neuronal abnormalities and amyloid deposits. Am J Pathol 1990; 137: 1383-92.
93. Nakamura S, Nakayama H, Goto N, et al. Histopathological studies of senile plaques and cerebral amyloidosis in cynomolgus monkeys. J Med Primatol 1998; 27: 244-52.
94. Uno H, Alsum PB, Dong S, et al. Cerebral amyloid angiopathy and plaques, and visceral amyloidosis in aged macaques. Neurobiol Aging 1996; 17: 275-81.
95. Nakamura S, Kiatipattanasakul W, Nakayama H, Ono F, Sakakibara I, Yoshikawa Y, Goto N, Doi K. Immunohistochemical characteristics of the constituents of senile plaques and amyloid angiopathy in aged cynomolgus monkeys. J Med Primatol 1996; 25: 294-300.
96. Oikawa N, Kimura N, Yanagisawa K. Alzheimer-type tau pathology in advanced aged nonhuman primate brains harboring substantial amyloid deposition. Brain Res 2010; 1315: 137-49.
97. Warzok RW, Kessler C, Apel G, et al. Apolipoprotein E4 promotes incipient Alzheimer pathology in the elderly. Alzheimer Dis Assoc Disord 1998; 12: 33-9.
98. Walker LC, Pahnke J, Madauss M, et al. Apolipoprotein E4 promotes the early deposition of Abeta42 and then Abeta40 in the elderly. Acta Neuropathol 2000; 100: 36-42.
99. Lemere CA, Beierschmitt A, Iglesias M, et al. Alzheimer's disease abeta vaccine reduces central nervous system abeta levels in a nonhuman primate, the Caribbean vervet. Am J Pathol 2004; 165: 283-97.
100. Nakamura S, Okabayashi S, Ageyama N, et al. Transthyretin amyloidosis and two other aging-related amyloidoses in an aged vervet monkey. Vet Pathol 2008; 45: 67-72.
101. Nakamura S, Tamaoka A, Sawamura N, et al. Carboxyl endspecific monoclonal antibodies to amyloid beta protein (A beta) subtypes (A beta 40 and A beta 42(43)) differentiate A beta in senile plaques and amyloid angiopathy in brains of aged cynomolgus monkeys. Neurosci Lett 1995; 201: 151-4.
102. Schultz C, Dehghani F, Hubbard GB, et al. Filamentous tau pathology in nerve cells, astrocytes, and oligodendrocytes of aged baboons. J Neuropathol Exp Neurol 2000; 59: 39-52.
103. Nelson PT, Stefansson K, Gulcher J, Saper CB. Molecular evolution of tau protein: implications for Alzheimer's disease. J Neurochem 1996; 67: 1622-32.
104. Hartig W, Klein C, Brauer K, et al. Abnormally phosphorylated protein tau in the cortex of aged individuals of various mammalian orders. Acta Neuropathol 2000; 100: 305-12.
105. Schultz C, Hubbard GB, Rub U, Braak E, Braak H. Age-related progression of tau pathology in brains of baboons. Neurobiol Aging 2000; 21: 905-12.
106. Braak H, Braak E, Bohl J, Bratzke H. Evolution of Alzheimer's disease related cortical lesions. J Neural Transm Suppl 1998; 54: 97-106.
107. Belleville S, Sylvain-Roy S, de Boysson C, Menard MC. Characterizing the memory changes in persons with mild cognitive impairment. Prog Brain Res 2008; 169: 365-75.
108. Presty SK, Bachevalier J, Walker LC, et al. Age differences in recognition memory of the rhesus monkey (Macaca mulatta). Neurobiol Aging 1987; 8: 435-40.
109. Moss MB, Rosene DL, Peters A. Effects of aging on visual recognition memory in the rhesus monkey. Neurobiol Aging 1988; 9: 495-502.
110. Sloane JA, Pietropaolo MF, Rosene DL, et al. Lack of correlation between plaque burden and cognition in the aged monkey. Acta Neuropathol 1997; 94: 471-8.
111. Herndon JG, Moss MB, Rosene DL, Killiany RJ. Patterns of cognitive decline in aged rhesus monkeys. Behav Brain Res 1997; 87: 25-34.
112. Jones B, Mishkin M. Limbic lesions and the problem of stimulus-reinforcement associations. Experimental Neurology 1972; 36: 362-77.
113. Rapp PR, Amaral DG. Evidence for task-dependent memory dysfunction in the aged monkey. J Neurosci 1989; 9: 3568-76.
114. Bachevalier J, Landis LS, Walker LC, et al. Aged monkeys exhibit behavioral deficits indicative of widespread cerebral dysfunction. Neurobiol Aging 1991; 12: 99-111.
115. Lai ZC, Moss MB, Killiany RJ, Rosene DL, Herndon JG. Executive system dysfunction in the aged monkey: spatial and object reversal learning. Neurobiol Aging 1995; 16: 947-54.
116. Moore TL, Killiany RJ, Herndon JG, Rosene DL, Moss MB. Impairment in abstraction and set shifting in aged rhesus monkeys. Neurobiol Aging 2003; 24: 125-34.
117. Moore TL, Killiany RJ, Herndon JG, Rosene DL, Moss MB. Executive system dysfunction occurs as early as middle-age in the rhesus monkey. Neurobiol Aging 2006; 27: 1484-93.
118. Braak H, Braak E. Diagnostic criteria for neuropathologic assessment of Alzheimer's disease. Neurobiol Aging 1997; 18: S85-8.
119. Walker ML, Anderson DC, Herndon JG, Walker LC. Ovarian aging in squirrel monkeys (Saimiri sciureus). Reproduction 2009; 138: 793-9.
120. Levy E, Amorim A, Frangione B, Walker LC. beta-Amyloid precursor protein gene in squirrel monkeys with cerebral amyloid angiopathy. Neurobiol Aging 1995; 16: 805-8.
121. Williams L. Aging Cebidae. Karger: Basel 2008.
122. Walker LC, Masters C, Beyreuther K, Price DL. Amyloid in the brains of aged squirrel monkeys. Acta Neuropathol 1990; 80: 381-7.
123. Walker LC, Kitt CA, Schwam E, et al. Senile plaques in aged squirrel monkeys. Neurobiol Aging 1987; 8: 291-6.
124. Elfenbein HA, Rosen RF, Stephens SL, et al. Cerebral betaamyloid angiopathy in aged squirrel monkeys. Histol Histopathol 2007; 22: 155-67.
125. Chambers JK, Kuribayashi H, Ikeda S, Une Y. Distribution of neprilysin and deposit patterns of Abeta subtypes in the brains of aged squirrel monkeys (Saimiri sciureus). Amyloid 2010; 17: 75-82.
126. Sawamura N, Tamaoka A, Shoji S, Koo EH, Walker LC, Mori H. Characterization of amyloid beta protein species in cerebral amyloid angiopathy of a squirrel monkey by immunocytochemistry and enzyme-linked immunosorbent assay. Brain Res 1997; 764: 225-9.
127. Maclean CJ, Baker HF, Ridley RM, Mori H. Naturally occurring and experimentally induced beta-amyloid deposits in the brains of marmosets (Callithrix jacchus). J Neural Transm 2000; 107: 799-814.
128. Geula C, Nagykery N, Wu CK. Amyloid-beta deposits in the cerebral cortex of the aged common marmoset (Callithrix jacchus): in cidence and chemical composition. Acta Neuropathol 2002; 103: 48-58.
129. Lemere CA, Oh J, Stanish HA, et al. Cerebral amyloid-beta protein accumulation with aging in cotton-top tamarins: a model of early Alzheimer's disease? Rejuvenation Res 2008; 11: 321-32.
130. Walker LC. Animal models of cerebral beta-amyloid angiopathy. Brain Res Brain Res Rev 1997; 25: 70-84.
131. Levy E, Carman MD, Fernandez-Madrid IJ, et al. Mutation of the Alzheimer's disease amyloid gene in hereditary cerebral hemorrhage, Dutch type. Science 1990; 248: 1124-6.
132. Bell RD, Zlokovic BV. Neurovascular mechanisms and bloodbrain barrier disorder in Alzheimer's disease. Acta Neuropathol 2009; 118: 103-13.
133. Morelli L, Wei L, Amorim A, et al. Cerebrovascular amyloidosis in squirrel monkeys and rhesus monkeys: apolipoprotein E genotype. FEBS Lett 1996; 379: 132-4.
134. Wei LH, Walker LC, Levy E. Cystatin C. Icelandic-like mutation in an animal model of cerebrovascular beta-amyloidosis. Stroke 1996; 27: 2080-5.
135. Graffagnino C, Herbstreith MH, Schmechel DE, Levy E, Roses AD, Alberts MJ. Cystatin C mutation in an elderly man with sporadic amyloid angiopathy and intracerebral hemorrhage. Stroke 1995; 26: 2190-3.
136. Palazzi X, Switzer R, George C. Natural occurrence of amyloid- Abeta deposits in the brain of young common marmosets (Callithrix jacchus): a morphological and immunohistochemical evaluation. Vet Pathol 2006; 43: 777-9.
137. Lyons DM, Yang C, Eliez S, Reiss AL, Schatzberg AF. Cognitive correlates of white matter growth and stress hormones in female squirrel monkey adults. J Neurosci 2004; 24: 3655-62.
138. Bartus RT, Dean RL, Beer B. Memory deficits in aged cebus monkeys and facilitation with central cholinomimetics. Neurobiology of Aging 1980; 1: 145-152.
139. Bons N, Rieger F, Prudhomme D, Fisher A, Krause KH. Microcebus murinus: a useful primate model for human cerebral aging and Alzheimer's disease? Genes Brain Behav 2006; 5: 120-30.
140. Silhol S, Calenda A, Jallageas V, Mestre-Frances N, Bellis M, Bons N. beta-Amyloid protein precursor in Microcebus murinus: genotyping and brain localization. Neurobiol Dis 1996; 3: 169-82.
141. Bons N, Jallageas V, Silhol S, Mestre-Frances N, Petter A, Delacourte A. Immunocytochemical characterization of Tau proteins during cerebral aging of the lemurian primate Microcebus murinus. C R Acad Sci III 1995; 318: 77-83.
142. Bons N, Mestre N, Petter A. Senile plaques and neurofibrillary changes in the brain of an aged lemurian primate, Microcebus murinus. Neurobiol Aging 1992; 13: 99-105.
143. Bons N, Mestre N, Ritchie K, Petter A, Podlisny M, Selkoe D. Identification of amyloid beta protein in the brain of the small, short-lived lemurian primate Microcebus murinus. Neurobiol Aging 1994; 15: 215-20.
144. Dhenain M, Michot JL, Privat N, et al. MRI description of cerebral atrophy in mouse lemur primates. Neurobiol Aging 2000; 21: 81-8.
145. Mestre-Frances N, Keller E, Calenda A, Barelli H, Checler F, Bons N. Immunohistochemical analysis of cerebral cortical and vascular lesions in the primate Microcebus murinus reveal distinct amyloid beta1-42 and beta1-40 immunoreactivity profiles. Neurobiol Dis 2000; 7: 1-8.
146. Kraska A, Dorieux O, Picq JL, et al. Age-associated cerebral atrophy in mouse lemur primates. Neurobiol Aging 2011; (Epub 2009); 32: 894-906.
147. Picq JL. Aging affects executive functions and memory in mouse lemur primates. Exp Gerontol 2007; 42: 223-32.
148. Picq JL, Aujard F, Volk A, Dhenain M. Age-related cerebral atrophy in nonhuman primates predicts cognitive impairments. Neurobiol Aging 2010.
149. Palop JJ, Mucke L. Amyloid-beta-induced neuronal dysfunction in Alzheimer's disease: from synapses toward neural networks. Nat Neurosci 2010; 13: 812-8.