Quantitative analysis of tau protein-immunoreactive accumulations and β amyloid protein deposits in the cerebral cortex of the mouse lemur, Microcebus murinus

Acta Neuropathologica

Volumn 94, Issue 2, 1997, Pages 131-139

  Giannakopoulos, P ^a   Silhol, S ^b   Jallageas, V ^b   Mallet, J ^c   Bons, N ^b   Bouras, C ^a   Delaere P ^d  

^a Department of Psychiatry ^*  (Switzerland)

^b PSL RESEARCH UNIVERSITY   (France)

^c PITIÉ SALPÊTRIÈRE HOSPITAL   (France)

^d SANOFI   (France)

Author keywords

Alzheimer's disease; Amyloid deposits; Mouse lemur; Primates; Tau protein

Indexed keywords

AMYLOID BETA PROTEIN; TAU PROTEIN;

AGING; ALZHEIMER DISEASE; AMYGDALOID NUCLEUS; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BIOCHEMISTRY; BRAIN CORTEX; CONTROLLED STUDY; ENTORHINAL CORTEX; FEMALE; HIPPOCAMPUS; MALE; NEOCORTEX; NEUROFIBRILLARY TANGLE; NEUROPROTECTION; NONHUMAN; PRIORITY JOURNAL; PROSIMIAN; PROTEIN ANALYSIS; SPECIES DIFFERENCE; SUBICULUM;

AGE FACTORS; ALZHEIMER DISEASE; AMYLOID BETA-PROTEIN; ANIMALS; CEREBRAL CORTEX; CHEIROGALEIDAE; DISEASE MODELS, ANIMAL; FEMALE; IMMUNOHISTOCHEMISTRY; MALE; REGRESSION ANALYSIS; TAU PROTEINS; TISSUE DISTRIBUTION;

EID: 0030751791     PISSN: 00016322     EISSN: None     Source Type: Journal    
DOI: 10.1007/s004010050684     Document Type: Article

References (63)

1. Arriagada PV, Growdon JH, Hedley-Whyte T, Hyman BT (1992) Neurofibrillary tangles but not senile plaques parallel duration and severity of Alzheimer's disease. Neurology 42: 631-639
2. Arriagada PV, Marzloff K, Hyman BT (1992) Distribution of Alzheimer-type pathologic changes in non-demented elderly individuals matches the pattern in Alzheimer's disease. Neurology 42: 1681-1688
3. Ball MJ, MacGregor J, Fyfe IM, Rapoport SI, London ED (1983) Paucity of morphological changes in the brains of ageing Beagle dogs: further evidence that Alzheimer lesions are unique for primate central nervous system. Neurobiol Aging 4: 127-131
4. Bierer LM, Hof PR, Purohit DP, Carlin L, Perl DP (1995) Neocortical neurofibrillary tangles correlate with dementia severity in Alzheimer's disease. Arch Neurol 52: 81-88
5. Bons N, Mestre N, Petter A (1991) Senile plaques and neurofibrillary changes in the brain of an aged lemurian primate, Microcebus murinus. Neurobiol Aging 13: 99-105
6. Bons N, Mestre N, Ritchie K, Petter A, Podlisny M, Selkoe D (1994) Identification of amyloid beta protein in the brain of the small, short-lived lemurian primate Microcebus murinus. Neurobiol Aging 15: 215-220
7. Bons N, Jallageas V, Silhol S, Mestre-Frances N, Fetter A, Delacourte A (1995) Immunocytochemical characterization of tau proteins during cerebral aging of the lemurian primate Microcebus murinus. C R Acad Sci (Paris) 318: 77-83
8. Bons N, Jallageas V, Mestre-Frances N, Silhol S, Petter A, Delacourte A (1995) Microcebus murinus, a convenient laboratory animal model for the study of Alzheimer's disease. Alzheimer Res 1: 83-87
9. Bouras C, Hof PR, Morrison JH (1993) Neurofibrillary tangle densities in the hippocampal formation in a non-demented population define subgroups of patients with differential early pathologic changes. Neurosci Lett 153: 131-135
10. Bouras C, Hof PR, Giannakopoulos P, Michel JP, Morrison JH (1994) Regional distribution of neurofibrillary tangles and senile plaques in the cerebral cortex of elderly patients: a quantitative evaluation of a one-year autopsy population. Cereb Cortex 4: 138-150
11. Braak H, Braak E (1991) Neuropathological stageing of Alzheimer-related changes. Acta Neuropathol 82: 239-259
12. Braak H, Braak E, StrothJohann M (1994) Abnormally phosphorylated tau protein related to the formation of neurofibrillary tangles and neuropil threads in the cerebral cortex of sheep and goat. Neurosci Lett 171: 1-4
13. Cork LC, Powers RE, Selkoe DJ, Davies P, Geyer JJ, Price DL (1988) Neurofibrillary tangles and senile plaques in aged bears. J Neuropathol Exp Neurol 47: 629-641
14. Cork LC, Masters C, Beyreuther K, Price DL (1990) Development of senile plaques. Relationships of neuronal abnormalities and amyloid deposits. Am J Pathol 137: 1383-1392
15. Crystal H, Dickson D, Fuld P, Masur D, Scott R, Mehler, M, Masdeu J, Kawas C, Aronson M, Wolfson L (1988) Clinicopathological studies in dementia: non-demented subjects with pathologically confirmed Alzheimer's disease. Neurology 38: 1682-1687
16. Cummings BJ, Head E, Ruehl W, Milgram NW, Cotman CW (1996) The canine as an animal model of human aging and dementia. Neurobiol Aging 17: 259-268
17. Dayan AD (1977) Comparative neuropathology of ageing. Studies on the brains of 47 species of vertebrates. Brain 94: 31-42
18. De Lacoste MC, White CL III (1993) The role of cortical connectivity in Alzheimer's disease pathogenesis: a review and a model system. Neurobiol Aging 14: 1-16
19. Delacourte A, Flament S, Dibe EM, Hublau P, Sablonnière B, Hémon B, Scherrer V, Défossez A (1990) Pathological proteins Tau 64 and 69 are specifically expressed in the somatodendritic domain of the degenerating cortical neurons during Alzheimer's disease. Demonstration with a panel of antibodies against Tau proteins. Acta Neuropathol 80: 111-117
20. Delacourte A, Sautière P-E, Wattez A, Mourton-Gilles C, Petter A, Bons N (1995) Biochemical characterization of tau proteins during cerebral aging of the lemurian primate Microcebus murinus. C R Acad Sci (Paris) 318: 85-89
21. Dickson DW, Crystal HA, Mattiace LA, Masur DM, Blau AD, Davies P, Yen SH, Aronson MK (1992) Identification of normal and pathological aging in prospectively studied nondemented elderly humans. Neurobiol Aging 13: 179-189
22. Games D, Adams D, Alessandrini R, et al (1995) Alzheimer-type neuropathology in transgenic mice overexpressing V717F β-amyloid precursor protein. Nature 373: 523-527
23. Gearing M, Rebeck GW, Hyman BT, Tigges J, Mirra S (1994) Neuropathology and apolipoprotein E profile of aged chimpanzees: implications for Alzheimer's disease. Proc Natl Acad Sci USA 91: 9382-9386
24. Giannakopoulos P, Hof PR, Mottier S, Michel JP, Bouras C (1994) Neuropathological changes in the cerebral cortex of 1258 cases from a geriatric hospital: retrospective clinicopathological evaluation of a 10-year autopsy population. Acta Neuropathol 87: 456-468
25. Giorgio G, Verga L, Finazzi M, Pollo B, Tagliavini F, Frangione B, Bugiani O (1990) Cerebral preamyloid deposits and congophilic angiopathy in aged dogs. Neurosci Lett 114: 178-183
26. Higgins LS, Rodems JM, Catalano R, Quon D, Cordell B (1995) Early Alzheimer disease-like histopathology increases in frequency with age in mice transgenic for β-APP751. Proc Natl Acad Sci USA 92: 4402-4406
27. Hof PR, Morrison JH (1990) Quantitative analysis of a vulnerable subset of pyramidal neurons in Alzheimer's disease. II. Primary and secondary visual cortex. J Comp Neurol 301: 55-64
28. Hof PR, Cox K, Morrison JH (1990) Quantitative analysis of a vulnerable subset of pyramidal neurons in Alzheimer's disease. I. Superior frontal and inferior temporal cortex. J Comp Neurol 301:44-54
29. Hof PR, Bierer LM, Perl DP, Delacourte A, Buée L, Bouras C, Morrison JH (1992) Evidence for early vulnerability of the medial and inferior aspects of the temporal lobe in an 82-year-old patient with preclinical signs of dementia: regional and laminar distribution on neurofibrillary tangles and senile plaques. Arch Neurol 49: 946-953
30. Hubbard BM, Fenton GW, Anderson JMA (1990) A quantitative histological study of early clinical and preclinical Alzheimer's disease. Neuropathol Appl Neurobiol 16: 111-121
31. Ikeda K, Haga C, Kosaka K, Oyanagi S (1989) Senile plaque-like structures: observation of a probably unknown type of amyloid plaque by periodic acid-methenamine silver (PAM) electron microscopy. Acta Neuropathol 78: 137-142
32. Ishihara T, Gondo T, Takahashi M, Uchino F, Ikeda S-I, Allsop D, Imai K (1991) Immunohistochemical and immunoelectron microscopical characterization of cerebrovascular and senile plaque amyloid in aged dog's brains. Brain Res 548: 196-205
33. Joachim CL, Mori H, Selkoe DJ (1989) Amyloid β protein deposition in tissue other than brain in Alzheimer's disease. Nature 341: 226-230
34. Katzman R, Terry RD (1983) Normal aging of the nervous system. In: Katzman R, Terry RD (eds) The neurology of aging. Davis, Philadelphia, pp 15-50
35. Le Gros Clark WE (1931) The brain of Microcebus murinus. Proc Zool Soc 463-484
36. Lewis DA, Campbell MJ, Terry RD, Morrison JH (1987) Laminar and regional distribution of neurofibrillary tangles and neuritic plaques in Alzheimer's disease: a quantitative study of visual cortex and auditory cortices. J Neurosci 7: 1799-1808
37. Martin LJ, Sisodia SS, Koo EH, Cork LC, Dellovade TL, Weidemann A, Beyreuther K, Masters C, Price DL (1991) Amyloid precursor protein in aged nonhuman primates. Proc Natl Acad Sci USA 88: 1461-1465
38. Martin LJ, Pardo CA, Cork LC, Price DL (1994) 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 145: 1358-1381
39. Masliah E, Ellisman M, Carragher B, Mallory M, Young S, Hansen L, DeTeresa R, Terry RD (1992) Three-dimensional analysis of the relationship between synaptic pathology and neuropil threads in Alzheimer's disease. J Neuropathol Exp Neurol 51: 404-414
40. Miller FD, Hicks SP, D'Amato CJ, Landis JR (1984) A descriptive study of neuritic plaques and neurofibrillary tangles in an autopsy population. Am J Epidemiol 120: 331-341
41. Morris JC, McKeel JDW, Storandt M, Rubin EH, Price JL, Grant EA, Ball MJ, Berg L (1991) Very mild Alzheimer's disease: informant-based clinical, psychometric, and pathologic distinction from normal aging. Neurology 41: 469-478
42. Nelson PT, Greenberg SG, Saper CB (1994) Neurofibrillary tangles in the cerebral cortex of sheep. Neurosci Lett 170: 187-190
43. Orr HT, Clark BH (1995) Biology of disease: genetic approaches to pathogenesis of neurodegenerative disorders. Lab Invest 73: 161-171
44. Pearson RCA, Esiri MM, Hiorns RW, Wilcock GK, Powell TPS (1985) Anatomical correlates of the distribution of the pathological changes in the neocortex in Alzheimer's disease. Proc Natl Acad Sci USA 82: 4531-4534
45. Peters A (1991) Aging in monkey cerebral cortex. Normal and altered states of function. In: Peters A, Jones EG (eds) Cerebral cortex. Plenum Press, New York, pp 485-510
46. Podlisny MB, Tolan DR, Selkoe DJ (1991) Homology of the amyloid β protein precursor in monkey and human supports a primate model for β amyloidosis in Alzheimer's disease. Am J Pathol 138: 1423-1435
47. Price DL, Cork LC, Struble RG, Kitt CA, Price DL Jr, Lehmann J, Hedreen JC (1985) Neuropathological, neurochemical, and behavioral studies of the aging nonhuman primate. Behavior and pathology of aging in rhesus monkeys. In: Davis RT, Leathers CW (eds) Monograhs in primatology. Liss, New York, pp 113-135
48. Price JL, Davis PB, Morris JC, White DL (1991) The distribution of tangles, plaques and related immunohistochemical markers in healthy aging and Alzheimer's disease. Neurobiol Aging 12: 295-312
49. Roertgen KE, Parisi JE, Clark BH, Barnes DL, O'Brien TD, Johnson KH (1996) Aβ-associated cerebral angiopathy and senile plaques with neurofibrillary tangles and cerebral hemorrhage in an aged wolverine (Gulo gulo). Neurobiol Aging 17: 243-247
50. Rogers J, Morrison JH (1985) Quantitative morphology and regional and laminar distributions of senile plaques in Alzheimer's disease. J Neurosci 5: 2801-2808
51. Russell MJ, Bobik M, White RG, Hou Y, Benjamin SA, Geddes JW (1996) Age-specific onset of β-amyloid in beagle brains. Neurobiol Aging 17: 269-273
52. Shimada A, Kuwamura M, Umemura T, Takada K, Ohama E, Itakura S (1991) Modified Bielschowsky and immunohistochemical studies on senile plaques in aged dogs. Neurosci Lett 129: 25-28
53. Struble RG, Price DL Jr, Cork LC, Price DL (1985) Senile plaques in cortex of aged normal monkeys. Brain Res 361: 267-275
54. Tekirian TL, Cole GM, Russell MJ, Yang F, Wekstein DR, Patel E, Snowdon DA, Markesbery WR, Geddes JW (1996) Carboxy terminal of β-amyloid deposits in aged human, canine, and polar bear brains. Neurobiol Aging 17: 249-257
55. Tomlinson BE (1972) Morphological brain changes in non-demented old people. In: Van Praag HM, Kalverboer AK (eds) Aging of the nervous system. DeErvon-Bohn, New York, pp 44-55
56. Tomlinson BE, Blessed G, Roth M (1968) Observations on the brains of non-demented old people. J Neurol Sci 7: 331-356
57. Uno H, Alsum PB, Dong S, Richardson R, Zimbric ML, Thieme CS, Houser WD (1996) Cerebral amyloid angiopathy and plaques, and visceral amyloidosis in aged macaques. Neurobiol Aging 17: 275-281
58. Vaughan DW, Peters A (1981) The structure of neuritic plaques in the cerebral cortex of aged rats. J Neuropathol Exp Neurol 40: 472-487
59. Vickers JC, Morrison JH, Friedrich VL Jr, Elder GA, Perl DP, Katz RN, Lazzarini RA (1994) Age-associated and cell-type-specific neurofibrillary pathology in transgenic mice expressing the human midsized neurofilament subunit. J Neurosci 14: 5603-5612
60. Walker LC, Kitt CA, Schwam E, Buckward F, Garcia F, Sepinwall J, Price DL (1987) Senile plaques in aged squirrel monkeys. Neurobiol Aging 8: 291-296
61. Walker LC, Kitt CA, Struble RG, Wagster MV, Price DL, Cork LC (1988) The neural basis of memory decline in aged monkeys. Neurobiol Aging 9: 657-666
62. Wisniewski HM, Johnson AB, Raine CS, Kay WJ, Terry RD (1970) Senile plaques and cerebral amyloidosis in aged dogs. A histochemical and ultrastructural study. Lab Invest 23: 287-296
63. Wisniewski HM, Ghetti B, Terry RD (1973) Neuritic (senile) plaques and filamentous changes in aged rhesus monkeys. J Neuropathol Exp Neurol 32: 566-584