Progression of neurofibrillary changes and PHF-τ in end-stage Alzheimer's disease is different from plaque and cortical microglial pathology

Neurobiology of Aging

Volumn 19, Issue 6, 1998, Pages 517-525

  Thal, Dietmar Rudolf ^a,b   Arendt, Thomas ^a   Waldmann, Guido ^a   Holzer, Max ^a   Zedlick, Dyrk ^a   Rüb, Udo ^b   Schober, Ralf ^a,c  

^a UNIVERSITY OF LEIPZIG   (Germany)

^b GOETHE UNIVERSITY   (Germany)

^c Institut fur Pathologie   (Germany)

Author keywords

Alzheimer's disease; Dementia rating; Neurofibrillary tangles; PHF ; Senile plaques

Indexed keywords

AMYLOID BETA PROTEIN; AMYLOID PRECURSOR PROTEIN; APOLIPOPROTEIN E; TAU PROTEIN;

ADULT; AGED; ALZHEIMER DISEASE; ARTICLE; AUTOPSY; CONTROLLED STUDY; CYTOSKELETON; ENZYME LINKED IMMUNOSORBENT ASSAY; FEMALE; HUMAN; HUMAN TISSUE; MAJOR CLINICAL STUDY; MALE; MICROGLIA; NEUROFIBRILLARY TANGLE; NEUROPIL THREAD; PATHOLOGY; PRIORITY JOURNAL; SENILE PLAQUE;

AGED; AGED, 80 AND OVER; ALZHEIMER DISEASE; AMYLOID BETA-PROTEIN PRECURSOR; ENZYME-LINKED IMMUNOSORBENT ASSAY; HUMANS; IMMUNOHISTOCHEMISTRY; MICROGLIA; MIDDLE AGED; NEUROFIBRILLARY TANGLES; SENILE PLAQUES; TAU PROTEINS;

EID: 0032460625     PISSN: 01974580     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0197-4580(98)00090-6     Document Type: Article

References (78)

1. 1. Akiyama, H.; Schwab, C.; Kondo, H.; Mori, H.; Kametani, F.; Ikeda, K.; McGeer, P. L. Granules in glial cells of patients with Alzheimer's disease are immunopositive for C-terminal sequenes of β-amyloid protein. Neurosci. Lett. 206:169-172; 1996.
2. 2. Alford, M. F.; Masliah, E.; Hansen, L. A.; Terry, R. D. A simple dot immunobinding assay for quantification of synaptophysin-like immunoreactivity in human brain. J. Histochem. Cytochem. 42:283-287; 1994.
3. 3. Arriagada, P. V.; Growdon, J. H.; Hedley-Whyte, E. T.; Hyman, B. T. Neurofibrillary tangles but not senile plaques parallel duration and severity of Alzheimer's disease. Neurology 42:631-639; 1992.
4. 4. Ball, M. J. Neuronal loss, neurofibrillary tangles and granulovacuolar degeneration in the hippocampus with ageing and dementia. A quantitative study. Acta Neuropathol. 37:111-118; 1977.
5. 5. Bancher, C.; Braak, H.; Fischer, P.; Jellinger, K. A. Neuropathological staging of Alzheimer lesions and intellectual status in Alzheimer's and Parkinson's disease patients. Neurosci. Lett. 162:179-182; 1993.
6. 6. Bancher, C.; Jellinger, K.; Lassmann, H.; Fischer, P.; Leblhuber, F. Correlation between mental state and quantitative neuropathology in the Vienna longitudinal study on dementia. Eur. Arch. Psychiatry Clin. Neurosci. 246:137-146; 1996.
7. 7. Berg L. Clinical dementia rating (CDR). Psychopharmacol. Bull. 24:637-639; 1988.
8. 8. 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. 56:414-420; 1997.
9. 9. Braak, E.; Braak, H.; Mandelkow, E.-M. A sequence of cytoskeleton changes related to the formation of neurofibrillary tangles and neuropil threads. Acta Neuropathol. 87:554-567; 1994.
10. 10. Braak, H.; Braak, E. Neuropathological stageing of Alzheimer-related changes. Acta Neuropathol. 82:239-259; 1991.
11. 11. Braak, H.; Braak, E. Pathology of Alzheimer's disease. In: Calne, D. B., ed. Neurodegenerative Diseases. Philadelphia: Saunders; 1994: 585-613.
12. 12. Braak, H.; Braak, E.; Yilmazer, D.; de Vos, R. A. J.; Jansen, E. N. H.; Bohl, J. Pattern of brain destruction in Parkinson's and Alzheimer's diseases. J. Neural. Transm. 103:455-490; 1996.
13. 13. Brückner, M.; Bendix, U.; Hube, M.; Arendt, T.; Bigl, V. Alzheimer's disease: A monoclonal antibody raised against paired helical filaments. Acta Histochem. 41:143-152; 1992.
14. 14. Cummings, B. J.; Cotman, C. W. Image analysis of beta-amyloid load in Alzheimer's disease and relation to dementia. Lancet 346:1524-1528; 1995.
15. 15. DeLacoste, M.-C.; White, C. L. The role of cortical connectivity in Alzheimer's disease pathogenesis: A review and model system. Neurobiol. Aging 14:1-16; 1993.
16. 16. DeKosky, S. T.; Scheff, S. W. Synapse loss in frontal cortex biopsies in Alzheimer's disease: Correlation with cognitive severity. Ann. Neurol. 27:457-464; 1990.
17. 17. Dickson, D. W. The pathogenesis of senile plaques. J. Neuropathol. Exp. Neurol. 56:321-339; 1997.
18. 18. Dickson, D. W. Neuropathological diagnosis of Alzheimer's disease: A perspective from longitudinal clinicopathological studies. Neurobiol. Aging 18:S21-S26; 1997.
19. 19. Dickson, D. W.; Crystal, H. A.; Mattiace, L. A.; Masur, D. M.; Blau, A. D.; Davies, P.; Yen, S.-H.; Aronson, M. K. Identification of normal and pathological aging in prospectively studied nondemented elderly humans. Neurobiol. Aging 13:179-189; 1991.
20. 20. Duyckaerts, C.; Delaère, P.; Hauw, J. J. Alzheimer's disease and neuroanatomy: Hypotheses and proposals. In: Boller, F.; Forette, F.; Khachatarian, Z; Poncet, M.; Christen, Y., eds. Heterogeneity of Alzheimer's Disease. Berlin: Springer; 1992:144-155.
21. 21. Duyckaerts, C.; Hauw, J. J. Diagnosis and staging of Alzheimer's disease. Neurobiol. Aging 18(S4):S33-S42; 1997.
22. 22. Folstein, M. F.; Folstein, S. E.; McHugh, P. R. Mini-mental state. A practical method for grading the cognitive state of patients for the clinician. J. Psychatr. Res. 12:189-198; 1975.
23. 23. Giulian, D.; Haverkamp, L. J.; Yu, J. H.; Karshin, W.; Tom, D.; Li, J.; Kirkpatrick, J.; Kuo, Y.-M.; Roher, A. E. Specific domains of β-amyloid from Alzheimer plaque elicit neuron killing in human microglia. J. Neurosci. 16:6021-6037; 1997.
24. 24. Goedert, M.; Strittmatter, W. J.; Roses, A. D. Risky apolipoprotein in brain. Nature 372:45-46; 1994.
25. 25. Greenberg, S. G. and Davies, P. A preparation of Alzheimer paired helical filaments that display distint tau proteins by polyacrylamide gel electrophoresis. Proc. Natl. Acad. Sci. 87:5827-5831; 1990.
26. 26. Griffin, W. S. T.; Stanley, L. C.; Ling, C.; White, L.; MacLeod, V.; Perrot, L.; White, C. L., III; Araoz, C. Brain interleukin-I and S100 immunoreactivity elevated in Down's syndrome and Alzheimer's disease. Proc. Natl. Acad. Sci. USA 86:7611-7615; 1989.
27. 27. Griffin, W. S. T.; Sheng, J. G.; Roberts, G. W.; Mrak, R. E. Interleukin-I expression in different plaque types in Alzheimer's disease: Significance in plaque evolution. J. Neuropath. Exp. Neurol. 54:276-281; 1995.
28. 28. Hardy, J. An "anatomical cascade hypothesis" for Alzheimer's disease. Trends Neurosci. 15:200-201; 1992.
29. 29. Hardy, J. Amyloid, the presinilins and Alzheimer's disease. Trends Neurosci. 20:154-159; 1997.
30. 30. Hof, P. R.; Morrison, J. H. The cellular basis of cortical disconnection in Alzheimer's disease and related dementing conditions. In: Terry, R. D.; Katzman, R.; Bick, K. L., eds. Alzheimer's Disease. New York: Raven Press; 1994:197-229.
31. 31. Holzer, M.; Holzapfel, H.-P.; Zedlick, D.; Brückner, M. K.; Arendt, T. Abnormally phosphorylated τ protein in Alzheimer's disease: Heterogeneity of individual regional distribution and relationship to clinical severity. Neuroscience 63:499-516; 1994.
32. 32. Hughes, C. P.; Berg, L.; Danziger, W. L.; Coben, L. A.; Martin, R. L. A new clinical scale for the staging of dementia. Br. J. Psychiat. 140:566-572; 1982.
33. 33. Hyman, B. T. The neuropathological diagnosis of Alzheimer's disease: Clinical-pathological studies. Neurobiol. Aging 18:S27-S32; 1997.
34. 34. Hyman, B. T.; Damasio, H.; Damasio, A. R.; Van Hoesen, G. W. Alzheimer's disease. Ann. Rev. Public Health 10:115-140; 1989.
35. 35. Hyman, B. T.; West, H. L.; Gomez-Isla, T.; Mui, S. Quantitative neuropathology in Alzheimer's disease: Neuronal loss in high-order association cortex parallels dementia. In: Iqbal, K.; Mortimer, J. A.; Winblad, B.; Wisniewski, H. M., eds. Research Advances in Alzheimer's Disease and Related Disorders. New York: Wiley & Sons; 1995;453-460.
36. 36. Hyman, B. T.; Wets, H. L.; Rebeck, G. W.; Buldyrev, S. V.; Mantegna, R. N.; Ukleja, M.; Havlin, S.; Stanley, H. E. Quantitative analysis of senile plaques in Alzheimer's disease: Observation of log-normal size distribution and molecular epidemiology of differences associated with apoliproprotein E genotype and trisomy 21 (Down syndrome). Proc. Natl. Acad. Sci. USA 92:3586-3590; 1995.
37. 37. Locascio, J. L.; Growdon, J. H.; Corkin, S. Cognitive test performance in detecting, staging and tracking Alzheimer's disease. Arch. Neurol. 52:1087-1099; 1995.
38. 38. März, W.; Scharnagl, H.; Kirca, M.; Bohl, J.; Groß, W.; Ohm, T. G. Apolipoprotein E polymorphism is associated with both senile plaque load and Alzheimer-type neurofibrillary tangle formation. Ann. N. Y. Acad. Sci. 777:276-280; 1996.
39. 39. Mattiace, L. A.; Davies, P.; Dickson, D. W. Detection of HLA-DR on microglia in the human brain is a function of both clinical and technical factors Am. J. Pathol. 136:1101-1114; 1990.
40. 40. McGeer, P. L.; Akiyama, H.; Itagaki, S.; McGeer, E. G. Immune system response in Alzheimer's disease. Can. J. Neurol. Sci. 16:516-527; 1989.
41. 41. McGeer, P. L.; Walker, D. G.; Akiyama, H.; Yasuhara, O.; McGeer, E. G. Involvement of microglia in Alzheimer's disease. Neuropathol. Appl. Neurobiol. 20:191-192; 1994.
42. 42. McKee, A. C.; Kosik, K. S.; Kowall, N. W. Neuritic pathology and dementia in Alzheimer's disease. Ann. Neurol. 30:156-165; 1991.
43. 43. Mirra, S. S.; Heyman, A.; McKeel, D.; Sumi, S. M.; Crain, B. J.; Brownlee, L. M.; Vogel, F. S.; Hughes, J. P.; van Belle, G.; Berg, L. and participating CERAD neuropathologists. The consortium to establish a registry for Alzheimer's, disease (CERAD). Part II. Standardization of the neuropathologic assessment of Alzheimer's disease. Neurology 41:479-486; 1991.
44. 44. Morris, J. C.; Heyman, A.; Mohs, R. C.; Hughes, J. P.; van Belle, G.; Fillenbaum, G.; Mellits, E. D.; Clark, C. and the CERAD investigators. The consortium to establish a registry for Alzheimer's disease (CERAD). Part I. Clinical and neuropsychological assessment of Alzheimer's disease. Neurology 39:1159-1165; 1989.
45. 45. Nagy, Zs.; Esiri, M. M.; Jobst, K. A.; Morris, J. H.; King, E. M.-F.; McDonald, B.; Litchfield, S.; Smith, A.; Barnetson, L.; Smith, A. D. Relative roles of plaques and tangles in the dementia of Alzheimer's disease: Correlations using three sets of neuropathological criteria. Dementia 6:21-31; 1995.
46. 46. Nagy, Zs.; Esiri, M. M.; Jobst, K. A.; Morris, J. H.; King, E. M.-F.; McDonald, B.; Joachim, C.; Litchfields, S.; Barnetson, L.; Smith, A. D. The effects of additonal pathology on the cognitive deficit in Alzheimer disease. J. Neuropathol. Exp. Neurol. 56:165-170; 1997.
47. 47. Namba, Y.; Tomonaga, M.; Kawasaki, H.; Otomo, E.; Ikeda, K. Apolipoprotein E immunoreactivity in cerebral amyloid deposits and neurofibrillary tangles in Alzheimer's disease and kuru plaque amyloid in Creutzfeldt-Jakob disease. Brain. Res. 541:163-166; 1991.
48. 48. The National Institute on Aging; Reagan Institute Working Group on Diagnostic Criteria for the Neuropathological Assessmant of Alzheimer's Disease. Consensus recommendations for the postmortem diagnosis of Alzheimer's disease. Neurobiol. Aging 18:S1-S2; 1997.
49. 49. Ohm, T. G.; Kirca, M.; Bohl, J.; Scharnagl, H.; Groß, W.; März, W. Apolipoprotein E polymorphism influences not only cerebral senile plaque load but also Alzheimer-type neurofibrillary tangle formation. Neuroscience 66:583-587; 1995.
50. 50. Perl, D. P.; Purohit, D. P.; Haroutunian, V. Clinicopathologic correlations of the Alzheimer's disease staging system introduced by Braak and Braak. J. Neuropathol. Exp. Neurol. 56:577; 1997.
51. 51. Price, J. L.; Davis, P. B.; Morris, J. C.; White, D. L. The distribution of tangles, plaques and related immunohistochemical markers in healthy aging and Alzheimer's disease. Neuobiol. Aging 12:295-312; 1991.
52. 52. Rebeck, G. W.; Reiter, J. S.; Strickland, D. K.; Hyman, B. T. Apolipoprotein E in sporadic Alzheimer disease: Allelic variation and receptor interactions. Neuron 11-575-580; 1993.
53. 53. Rebeck, G. W.; Harr, S. D.; Strickland, D. K.; Hyman, B. T. Multiple, diverse senile plaque-associated proteins are ligands of an apolipoprotein E receptor, the α2-Macroglobulin receptor/Low density-lipoprotein receptor related protein. Ann. Neurol. 37:211-217; 1995.
54. 54. Reisberg, B.; Ferris, S. H.; de Leon, M. J.; Crook, T. The global deterioration scale for assessment of primary degenerative dementia. Am. J. Psychiatry 139:1136-1139; 1982.
55. 55. Reisberg, B.; Ferris, S. H.; de Leon, M. J.; Crook, T. Global deterioration scale (GDS). Psychopharmacol. Bull. 24:661-663; 1988.
56. 56. Roth, M.; Huppert, F. A.; Tym, E.; Mountjoy, C. Q. CAMDEX. The Cambridge examination for mental disorders in the elderly. Cambridge: Cambridge University Press; 1988.
57. 57. Schmechel, D. E.; Saunders, A. M.; Strittmatter, W. J.; Crain, B. J.; Hulette, C. M.; Joo, S. H.; Pericak-Vance, M. A.; Goldgaber, D.; Roses, A. D. Increased amyloid β-peptide deposition in cerebral cortex as a consequence of apolipoprotein E genotype in late-onset. Proc. Natl. Acad. Sci. USA 90:9649-9653; 1993.
58. 58. Schwab, C.; Steele, J. C.; McGeer, P. L. Neurofibrillary tangles of Guam Parkinson-dementia with reactive microglia and complement proteins. Brain Res. 707:196-205; 1996.
59. 59. Sheng, J. G.; Mrak, R. E.; Griffin, W. S. T. Apolipoprotein E distribution among different plaque types in Alzheimer's disease: Implications for its role in plaque progression. Neuropath. Appl. Neurobiol. 22:334-341; 1996.
60. 60. Sheng, J. G.; Mrak, R. E.; Griffin, W. S. T. Glial-neuronal interactions in Alzheimer disease: Progressive association of IL-1a4 microglia and S100b + astrocytes with neurofibrillary tangles stages. J. Neuropathol. Exp. Neurol. 56:285-290; 1997.
61. 61. Sheng, J. G.; Mrak, R. E.; Griffin, W. S. T. Neuritic plaque evolution in Alzheimer's disease is accompanied by transition of activated microglia from primed to enlarged to phagocytotic forms. Acta Neuropathol. 94:1-5; 1997.
62. 62. Terry, R. D.; Peck, A.; DeTeresa, R.; Schechter, R.; Horoupian, D. S. Some morphometric aspects of the brain in senile dementia of the Alzheimer's type. Ann. Neurol. 10:184-192; 1981.
63. 63. Terry, R. D.; Masliah, E.; Salmon, D. P.; Butters, N.; DeTeresa, R.; Hill, R.; Hansen, L. A.; Katzman, R. Physical basis of cognitive alterations in Alzheimer's disease: Synapse loss is the major correlate of cognitive impairment. Ann. Neurol. 30:572-580; 1991.
64. 64. Thal, D. R.; Glas, A.; Schneider, W.; Schober, R. Differential pattern of β-amyloid, amyloid precursor protein and apolipoprotein E expression in cortical senile plaques. Acta Neuropathol. 94:255-265; 1997.
65. 65. Thal, D. R.; Schober, R. Glial cell reactions in the aging brain and in Alzheimer's disease. Clin. Neuropathol. 16:292; 1997.
66. 2-macroglobulin and interleukin 6 in Alzheimer's disease. Brain Res. 777:223-227; 1997.
67. 67. Uchihara, T.; Duyckaerts, C.; He, Y.; Kobayashi, K.; Seilhean, D.; Amouyel, P.; Hauw, J.-J. Apo E immunoreactivity and microglial cells in Alzheimer's disease brain. Neurosci. Lett. 195:5-8; 1995.
68. 68. Uchihara, T.; Duyckaerts, C.; Lazarini, F.; Mokhtari, K.; Seilhean, D.; Amouyel, P.; Hauw, J.-J. Inconstant apolipoprotein E (Apo E)-like immunoreactivity in amyloid β protein deposits: relationship with Apo E genotype in aging brain and Alzheimer's disease. Acta Neuropathol. 92:180-185; 1996.
69. 69. Urmoneit, B.; Prikulis, I.; Wihl, G.; D'Urso, D.; Frank, R.; Heeren, J.; Beisiegel, U. Cerebrovascular smooth muscle cells internalize Alzheimer amyloid beta protein via a lipoprotein pathway: Implications for cerebral amyloid angiopathy. Lab. Invest. 77:157-166; 1997.
70. 70. Wang, D.; Munoz, D. G. Qualitative and quantitative differences in senile plaque dystrophic neurites of Alzheimer's disease and normal aged brain. J. Neuropathol. Exp. Neurol. 54:548-556; 1995.
71. 71. Welsh, K. A.; Butters, N.; Hughes, J. P.; Mohs, R. C.; Heyman, A. Detection and staging of dementia in Alzheimer's disease. Use of the neuropsychological measures developed for the consortium to establish a registry for Alzheimer's disease. Arch. Neurol. 49:448-452; 1992.
72. 72. Wisniewski, H. M.; Wegiel, J.; Wang, K. C.; Kujawa, M.; Lach, B. Ultrastructural studies of the cells forming amyloid fibres in classical plaques. Can. J. Neurol. Sci. 16:535-542; 1989.
73. 73. Wisniewski, H. M.; Vorbrodt, A. W.; Wegiel, J.; Morys, J.; Lossinsky, A. S. Ultrastructure of the cells forming amyloid fibers in Alzheimer disease and Scrapie. Am. J. Med. Gen. Suppl. 7:287-297; 1990.
74. 74. Wisniewski, H. M.; Wegiel, J.; Strojny, P.; Wang, K.-C.; Kim, K.-S.; Burrage, T. Ultrastructural morphology and immunocytochemistry of β amyloid classical, primitive and diffuse plaque. In: Ishii, T.; Allsop, D.; Selkoe, D., eds. Frontiers of Alzheimer disease. Amsterdam: Elsevier; 1991:99-108.
75. 75. Wisniewski, H. M.; Wegiel, J.; Kotula, L. Some neuropathological aspects of Alzheimer's disease and its relevance to other disciplines. Neuropathol. Appl. Neurobiol. 22:3-11; 1996.
76. 76. Wisniewski, T.; Frangione, B. Apolipoprotein E: A pathological chaperone protein in patients with cerebral and systemic amyloid. Neurosci. Lett. 135:235-238; 1992.
77. 77. Yasuhara, O.; Kawamata, T.; Aimi, Y ; McGeer, E. G.; McGeer, P. L. Two types of dystrophic neurites in senile plaques of Alzheimer's disease and elderly non-demented cases. Neurosci. 171:73-76; 1994.
78. 78. Yamaguchi, H.; Ishiguro, K.; Sugihara, S.; Nakazato, Y.; Kawarabayashi, T.; Sun, X.; Hirai, S. Presence of apolipoprotein E on extracellular neurofibrillary tangles and on meningeal blood vessels precedes the Alzheimer β-amyloid deposition. Acta Neuropathol. 88:413-419; 1994.