Are pathological lesions in neurodegenerative disorders the cause or the effect of the degeneration?

Neuropathology

Volumn 22, Issue 3, 2002, Pages 133-146

  Armstrong, Richard A ^a   Cairns, Nigel J ^b   Lantos, Peter L ^b  

^a ASTON UNIVERSITY   (United Kingdom)

^b KING'S COLLEGE LONDON   (United Kingdom)

Author keywords

Disease pathogenesis; Extracellular protein deposits; Intracellular inclusions; Neurodegenerative disorders; Pathological lesions

Indexed keywords

PROTEIN;

ALZHEIMER DISEASE; BRAIN DEGENERATION; CELL INCLUSION; CELL STRUCTURE; DEGENERATIVE DISEASE; EXTRACELLULAR SPACE; FRONTOTEMPORAL DEMENTIA; GENE MUTATION; HEAD INJURY; HUMAN; HYPOTHESIS; LEWY BODY; MOLECULAR BIOLOGY; NONHUMAN; PATHOGENESIS; PRIORITY JOURNAL; PROGRESSIVE SUPRANUCLEAR PALSY; REVIEW; TRANSGENICS;

ANIMALS; HUMANS; INCLUSION BODIES; NERVE DEGENERATION; NEURODEGENERATIVE DISEASES; NEURONS; SENILE PLAQUES;

EID: 0036711238     PISSN: 09196544     EISSN: None     Source Type: Journal    
DOI: 10.1046/j.1440-1789.2002.00446.x     Document Type: Review

References (105)

1. Delaere P, Duyckaerts C, He Y, Piette F, Hauw JJ. Subtypes and differential laminar distribution of β/A4 deposits in Alzheimer's disease: Relationship with the intellectual status of 26 cases. Acta Neuropathol 1991; 81: 328-335.
2. Armstrong RA. β-amyloid plaques: Stages in life history or independent origin? Dement Geriatr Cogn Disord 1998; 9: 227-238.
3. Glenner GG, Wong CW. Alzheimer's disease and Down's syndrome: Sharing of a unique cerebrovascular amyloid fibril protein. Biochem Biophys Res Commun 1984; 122: 1131-1135.
4. Yamaguchi H, Ishiguro K, Sugihara S et al. Presence of apolipoprotein ε on extracellular neurofibrillary tangles and on meningeal blood vessels precedes the Alzheimer β-amyloid deposition. Acta Neuropathol 1994; 88: 413-419.
5. Verga L, Frangione B, Tagliavini F, Giaccone G, Migheli A, Bugiani O. Alzheimer's and Down's patients: Cerebral preamyloid deposits differ ultrastructurally and histochemically from the amyloid of senile plaques. Neurosci Lett 1989; 105: 294-299.
6. Mann DMA, Brown SMP, Owen F, Baba M, Iwasubo T. Amyloid beta protein (Aβ) deposition in dementia with Lewy bodies. Predominance of Aβ42/43 and a paucity of Aβ40 compared with sporadic Alzheimer's disease. Neuropathol Appl Neurobiol 1988; 24: 187-194.
7. Fukuda T, Tanaka J, Watabe K, Numoto RT, Minamitani M. Immunohistochemistry of neuronal inclusions in the cerebral cortex and brain stem in Lewy body dementia. Acta Pathol Jpn 1993; 43: 545-551.
8. Gai WP, Blumbergs PC, Blessing WW. Microtubule-associated protein-5 is a component of Lewy bodies and Lewy body neurites in the brainstem and forebrain regions affected in Parkinson's disease. Acta Neuropathol 1996; 91: 78-81.
9. Brion JP, Couk AM. Cortical and brain stem type Lewy bodies are immunoreactive for the cyclin dependent kinase-5. Am J Pathol 1995; 147: 1465-1476.
10. Lowe J, Mayer RJ, Landon M. Ubiquitin in neurodegenerative diseases. Brain Pathol 1993; 3: 55-65.
11. Iwatsubo T, Yamaguchi H, Fujinuro M et al. Purification and characterisation of Lewy bodies from the brains of patients with diffuse Lewy body disease. Am J Pathol 1996; 148: 1517-1529.
12. Spillantini MG, Crowther RA, Jakes R, Cairns NJ, Lantos PL, Goedert M. Filamentous alpha-synuclein inclusions link multiple systems atrophy with Parkinson's disease and dementia with Lewy bodies. Neurosci Lett 1998; 251: 205-208.
13. Love S, Saitoh T, Quyada S, Cole GM, Terry RD. Ubiquitin and tau immunoreactivity of neurofibrillary tangles, Pick bodies and Lewy bodies. J Neuropathol Exp Neurol 1988; 47: 393-405.
14. Ksiezak-Reding H, Tracz E, Yang LS, Dickson DW, Simon M, Walt JS. Ultrastructural stability of paired helical filaments from corticobasal degeneration as examined by scanning transmission electron microscopy. Am J Pathol 1996; 149: 639-651.
15. Tracz E, Dickson DW, Hainfeld JF, Ksiezak-Reding H. Paired helical filaments in corticobasal degeneration: The fine fibrillary structure with NanoVan. Brain Res 1997; 773: 33-44.
16. Hardy JA, Higgins GA. Alzheimer's disease: The amyloid cascade hypothesis. Science 1992; 256: 184-185.
17. Jackson M, Lowe J. The new neuropathology of degenerative frontotemporal dementias. Acta Neuropathol 1996; 91: 127-134.
18. El Hachini KH, Cervenakova L, Brown P et al. Mixed features of Alzheimer's disease and Creutzfeldt-Jakob disease in a family with a presenilin 1 mutation in chromosome 14. Amyloid: Int J Exp Clin Inv 1996; 3: 223-233.
19. Grimes DA, Bergeron CB, Lang AE. Motor neuron disease: Inclusion dementia presenting as cortical basal ganglionic degeneration. Move Disord 1999; 14: 674-680.
20. Rubio A, Steinberg K, Figlewicz DA et al. Coexistence of Huntingdon's disease and familial amylotrophic lateral sclerosis: Case presentation. Acta Neuropathol 1996; 92: 421-427.
21. Armstrong RA. Diffuse β-amyloid (Aβ) deposits and neurons: In situ secretion or diffusion of Aβ? Alz Rep 2001a; 3: 289-294.
22. Giaccone G, Tagliavini F, Linol G, Bouras C, Frigerio L. Down's patients: Extracellular preamyloid deposits precede neuritic degeneration and senile plaques. Neurosci Lett 1989; 97: 232-238.
23. Armstrong RA. Dispersion of classic β-amyloid deposits around blood vessels in Alzheimer's disease. Alz Rep 2001b; 4: 103-108.
24. Schultz-Schaeffer WJ, Giese A, Windl O, Kretschmar HA. Polymorphism at codon 129 of the prion protein gene determines cerebellar pathology in Creutzfeldt-Jakob disease. Clin Neuropath 1996; 15: 353-357.
25. Ironside JW. Pathology of variant Creutzfeldt-Jakob disease. Arch Virol Suppl 2000; 16: 143-151.
26. Armstrong RA, Cairns NJ, Ironside JW, Lantos PL. Quantification of the vacuolation ('spongiform change'), surviving neurons, and prion protein deposition in eleven cases of variant Creutzfeldt-Jakob disease (vCJD). Acta Neuropathol 2001; 102: 591-596.
27. Komori T. Tau positive glial inclusions in progressive supranuclear palsy, corticobasal degeneration and Pick's disease. Brain Pathol 1999; 9: 663-679.
28. Tabaton M, Perry G, Gambetti L, Manello V, Gambetti P. Influence of neuronal location on antigenic properties of neurofibrillary tangles. Ann Neurol 1988; 23: 604-610.
29. Sergeant N, Wattez A, Delacourte A. Neurofibrillary degeneration in progressive supranuclear palsy and corticobasal degeneration: Tau pathologies with exclusively 'exon 10' isoforms. J Neurochem 1999; 72: 1243-1249.
30. Feany MB, Mattiace LA, Dickson DW. Neuropathologic overlap of progressive supranuclear palsy, Pick's disease and corticobasal degeneration. J Neuropath Exp Neurol 1996; 55: 53-67.
31. Buee L, Delacourte A. Comparative biochemistry of tau in progressive supranuclear palsy, corticobasal degeneration, fronto-temporal dementia with parkinosonism linked to chromosome 17, and Pick's disease. Brain Pathol 1999; 4: 681-693.
32. Buee-Scherrer V, Hof PR, Buee L et al. Hyperphosphorylated tau proteins differentiate corticobasal degeneration and Pick's disease. Acta Neuropathol 1996; 91: 351-359.
33. Cairns NJ, Atkinson PF, Hanger DP, Anderton BH, Daniel SE, Lantos PL. Tau protein in the glial cytoplasmic inclusions of multiple systems atrophy can be distinguished from abnormal tau in Alzheimer's disease. Neurosci Lett 1997; 230: 49-52.
34. Dickson DW, Liu WK, Hardy J et al. Widespread alterations of alpha-synuclein in multiple systems atrophy. Am J Pathol 1999; 155: 1241-1251.
35. Clayton DF, George JM. Synucleins in synaptic plasticity and neurodegenerative disorders. J Neurosci Res 1999; 58: 120-129.
36. Chartier-Harlin MC, Crawford F, Houlden H et al. Early onset Alzheimer's disease caused by mutations at codon 717 of the β-amyloid precursor protein gene. Nature 1991; 353: 844-846.
37. Goate R, Cartier-Harlin MC, Mullan M et al. Segregation of a missense mutation in the amyloid precursor protein gene with familial Alzheimer's disease. Nature 1991; 349: 704-706.
38. Games D, Adams D, Alessandrini R et al. Alzheimertype neuropathology in transgenic mice overexpressing V717F β-amyloid precursor protein. Nature 1995; 373: 523-527.
39. Lantos PL, Luthert PJ, Hanger D, Anderton BH, Mullan M, Rossor M. Familial Alzheimer's disease with the amyloid precursor protein position 717 mutation and sporadic Alzheimer's disease have the same cytoskeletal pathology. Neurosci Lett 1992; 137: 221-224.
40. Armstrong RA, Myers D, Smith CUM. The spatial patterns of β/A4 deposit subtypes in Alzheimer's disease. Acta Neuropathol 1993a; 86: 36-41.
41. Armstrong RA, Myers D, Smith CUM. The spatial patterns of plaques and tangles in Alzheimer's disease do not support the 'Cascade hypothesis'. Dementia 1993b; 4: 16-20.
42. Goldfarb LG, Brown P, Cervenakova L, Gajdusek DC. Genetic analysis of Creutzfeldt-Jakob disease and related disorders. Phil Trans Roy Soc Series B 1994; 343: 379-384.
43. Parchi P, Giese A, Capellari S et al. Classification of sporadic Creutzfeldt-Jakob disease based on molecular and phenotypic analysis of 300 subjects. Ann Neurol 1999; 46: 224-233.
44. MacDonald ST, Sutherland K, Ironside JW. Prion protein genotype and pathological phenotype studies in sporadic Creutzfeldt-Jakob disease. Neuropath Appl Neurobiol 1996; 22: 285-292.
45. Foster NL. Fronto-temporal dementia with parkinsonism linked to chromosome 17 (FTDP-17): A clinician's guide. Neurologist 1999; 5: 213-221.
46. Nasreddine ZS, Logimov M, Clark LN et al. From genotype to phenotype: A clinical, pathological and biochemical investigation of frontotemporal dementia and parkinsonism (FTDP-17) caused by the P301L tau mutation. Anns Neurol 1999; 45: 704-715.
47. Higgins JJ, Adler RL, Loveless JM. Mutational analysis of the tau gene in progressive supranuclear palsy. Neurology 1999; 53: 1421-1424.
48. Hoenicka J, Perez M, Perez-Tur J et al. The tau gene AO allele and progressive supranuclear palsy. Neurology 1999; 53: 1219-1225.
49. Gentleman SM, Nash MJ, Sweeting CJ, Graham DI, Roberts GW. β-amyloid precusor protein (βAPP) as a marker for axonal injury after head injury. Neurosci Lett 1993; 160: 139-144.
50. McKenzie JE, Gentleman SM, Roberts GW, Graham DI, Royston MC. Increased numbers of βAPP-immunoreactive neurons in the entorhinal cortex after head injury. Neuroreport 1994; 6: 161-164.
51. Roberts GW, Gentleman SM, Lynch A, Murray L, Landon M, Graham DI. β-amyloid protein deposition in the brain after severe head injury: Implications for the pathogenesis of Alzheimer's disease. J Neurol Neurosurg Psychiatr 1994; 57: 419-425.
52. Kalaria RN, Perry G. Amyloid P component and other acute-phase proteins associated with cerebellar Aβ deposits in Alzheimer's disease. Brain Res 1993; 631: 151-155.
53. Regland B, Gottfries CG. The role of amyloid βprotein in Alzheimer's disease. Lancet 1992; 340: 467-469.
54. Wisniewski T, Ghiso J, Frangione B. Alzheimer's disease and soluble Aβ. Neurobiol Aging 1994; 15: 143-152.
55. Renkawek K, Dejong WW, Merck KB, Frenken CWGM, van Workum FPA, Bosman GJCGM. Alpha-B-crystallin is present in reactive glia in Creutzfeldt-Jakob disease. Acta Neuropathol 1992; 83: 324-327.
56. Castellani R, Parchi P, Stahl J, Capellari S, Cohen M, Gambetti P. Early pathological and biochemical changes in Creutzfeldt-Jakob disease: Study of brain biopsies. Neurol 1996; 46: 1690-1693.
57. Carota A, Pizzolato GP, Gailloud P et al. A panencephalopathic type of Creutzfeldt-Jakob disease with selective lesions of the thalamic nuclei in two Swiss patients. Clin Neuropath 1996; 15: 125-134.
58. Arendash GW, Millard WJ, Dunn AJ, Meyer EM. Long term neuropathological and neurochemical effects of nucleus basalis lesions in the rat. Science 1987; 238: 952-956.
59. Wallace WC, Bragin V, Robakis NK et al. Increased biosynthesis of Alzheimer amyloid precursor protein in the cerebral cortex of rats with lesions of the nucleus basalis of Meynert. Mole Brain Res 1991; 10: 173-178.
60. Stephenson DT, Rash K, Clemens JA. Amyloid precursor protein accumulates in regions of neurodegeneration following focal cerebral ischemia in the rat. Brain Res 1992; 593: 128-135.
61. Kawarabayashi T, Shoji M, Harigaya Y, Yamaguchi H, Hirai S. Expression of amyloid precursor protein in early stage of brain damage. Brain Res 1991; 563: 334-338.
62. Kalaria RN, Bhatti SU, Perry G, Lust WD. The amyloid precursor protein in ischaemic brain injury and chronic hypoperfusion. Ann NY Acad Sci 1993; 695: 190-193.
63. Torack RM, Miller JW. Immunoreactive changes resulting from dopaminergic denervation of the dentate gyrus of the rat hippocampal formation. Neurosci Lett 1994; 169: 9-12.
64. Newell KL, Boyer P, Gomez-Tortosa E et al. Alphasynuclein immunoreactivity is present in axonal swellings in neuroaxonal dystrophy and acute traumatic brain injury. J Neuropath Exp Neurol 1999; 58: 1263-1268.
65. Kowall NW, Hantraye P, Brouillet E, Beal MF, McKee AC. MPTP induces alpha-synuclein aggregation in the substantia nigra of baboons. Neuroreport 2000; 11: 211-213.
66. Kowall NW, Beal MF, Busciglio J, Duffy LK, Yanker BA. An in vivo model for the neurodegenerative effects of β-amyloid and protection by substance P. Proc Natl Acad Sci USA 1991; 88: 7247-7251.
67. Doebler JA, Markesbury WR, Anthony A, Davies P, Scheff SW, Rhoads RE. Neuronal RNA: In relation to Alz50 immunoreactivity in Alzheimer's disease. Anns Neurol 1988; 23: 20-24.
68. Takashima A, Noguchi K, Sato K, Hoshino T, Imahori K. Tau protein kinase 1 is essential for amyloid βprotein induced neurotoxicity. Proc Natl Acad Sci USA 1993; 90: 7789-7793.
69. Bancher C, Lassmann H, Breitschopf H, Jellinger KA. Mechanisms of cell death in Alzheimer's disease. J Neural Transm (Suppl) 1997; 50: 141-152.
70. Sutton ET, Hellermann GR, Thomas T. Beta-amyloid induced endothelial necrosis and inhibition of nitric oxide production. Exp Cell Res 1997; 230: 368-376.
71. Behl C, Davis JB, Klier FG, Schubert D. Amyloidbeta peptide induces necrosis rather than apoptosis. Brain Res 1994; 645: 253-264.
72. Forloni G, Bertain I, Catella AM, Thaler F, Invernizzi R. Alpha-synuclein and Parkinson's disease: Selective neurodegenerative effect of alpha-synuclein fragment on dopaminergic neurons in vitro and in vivo. Anns Neurol 2000; 47: 632-640.
73. Betmouni S, Perry VH. The acute inflammatory response in central nervous system following injection of prion brain homogenate or normal brain homogenate. Neuropathol Appl Neurobiol 1999; 25: 20-28.
74. Su Y, Ni BH. Selective deposition of amyloid-beta protein in the entorhinal dentate projection of a transgenic mouse model of Alzheimer's disease. J Neurosci Res 1998; 53: 177-186.
75. Iryarry MC, McNamara M, Fedorchak K, Hsiao K, Hyman BT. APP (Sw) transgenic mice develop age related amyloid beta deposits and neuropil abnormalities but no neuronal loss in CA1. J Nettropathol Exp Neurol 1997; 56: 965-973.
76. Ichihara N, Wu J, Chui DH, Yamazuki K, Wakabayashi T, Kikuchi T. Axonal degeneration promotes abnormal accumulation of amyloid β-protein in ascending gracile axonal dystrophy (GAD) mouse. Brain Res 1995; 695: 173-178.
77. Zhou WB, Hurlbert MS, Schaack J, Prasad KN, Freed CR. Overexpression of human alpha-synuclein causes dopamine neuron death in rat primary culture and immortalized mesencephalon-derived cells. Brain Res 2000; 866: 33-43.
78. Masliah E, Rockenstein E, Veinbergs I et al. Dopaminergic loss and inclusion body formation in alphasynuclein mice: Implications for neurodegenerative disorders. Science 2000; 287: 1265-1269.
79. Struble RG, Powers RE, Casanova MF, Kitt CA, Brown EC, Price DL. Neuropeptidergic systems in plaques of Alzheimer's disease. J Neuropath Exp Neurol 1987; 46: 567-584.
80. Allsop D, Haga S, Haga C, Ikeda SI, Mann DMA, Ishii T. Early senile plaques in Down's syndrome brains show a close relationship with cell bodies of neurons. Neuropath Appl Neurobiol 1989; 15: 531-542.
81. Akiyama H, Tago H, Itagaki S, McGeer PL. Occurrence of diffuse amyloid deposits in the presubicular parvopyramidal layer in Alzheimer's disease. Acta Neuropathol 1990; 79: 537-544.
82. Ginsberg SD, Crino PB, Heinby SE et al. Predominance of neuronal mRNAs in individual Alzheimer's disease senile plaques. Anns Neurol 1999; 45: 174-181.
83. Adams LA, Munoz DG. Differential incorporation of processes derived from different classes of neurons into senile plaques in Alzheimer's disease. Acta Neuropathol 1993; 86: 365-370.
84. DeLacoste MC, White CL. The role of cortical connectivity in Alzheimer's disease pathogenesis: A review and model system. Neurobiol Aging 1993; 14: 1-16.
85. Pearson RCA, Esiri MM, Hiorns RW, Wilcock GK, Powell TPS. Anatomical correlates of the distribution of the pathological changes in the neocortex in Alzheimer's disease. Proc Natl Acad Sci USA 1985; 82: 4531-4534.
86. Hyman BT, Tanzi RE. Amyloid, dementia and Alzheimer's disease. Curr Opin Neurol Neurosurg 1992; 5: 88-93.
87. Senut MC, Roudier M, Davous P, Fallet-Bianco C, Lamour Y. Senile dementia of the Alzheimer type: Is there a correlation between entorhinal cortex and dentate gyrus lesions? Acta Neuropathol 1991; 82: 306-315.
88. Armstrong RA. Is the clustering of neurofibrillary tangles in Alzheimer's patients related to the cells of origin of specific cortico-cortical projections? Neurosci Lett 1993; 160: 57-60.
89. Armstrong RA. The spatial pattern of discrete βamyloid deposits in Alzheimer's disease reflects synaptic disconnection. Dementia 1996; 7: 86-90.
90. Kosaka K, Iseki E, Odawara T, Yamamoto T. Cerebral type of Lewy body disease. Neuropathology 1996; 16: 32-35.
91. Wakabayashi K, Honer WG, Masliah E. Synapse alterations in the hippocampal entorhinal formation in Alzheimer's disease with and without Lewy body disease. Brain Res 1994; 667: 24-32.
92. Kazee AM, Han LY. Cortical Lewy bodies in Alzheimer's disease. Arch Pathol Lab Med 1995; 119: 448-453.
93. Armstrong RA, Cairns NJ, Lantos PL. Dementia with Lewy bodies. Clustering of Lewy bodies in human patients. Neurosci Lett 1997; 224: 41-44.
94. Armstrong RA, Cairns NJ, Lantos PL. The spatial patterns of Lewy bodies, senile plaques and neurofibrillary tangles in Dementia with Lewy bodies. Exp Neurol 1998a; 150: 122-127.
95. Brun A, Passant U. Frontal lobe degeneration of the non-Alzheimer type: Structural characteristics, diagnostic criteria and relation to other frontotemporal dementias. Acta Neurol Scand 1996; 94: 28-30.
96. Ferrer I. Neurons and their dendrites in frontotemporal dementia. Dementia Geriatr Cog Disord 1999; 10: 55-60.
97. Armstrong RA, Cairns NJ, Lantos PL. Clustering of Pick bodies in patients with Pick's disease. Neurosci Lett 1998b; 242: 81-84.
98. Armstrong RA, Cairns NJ, Lantos PL. Clustering of cerebral cortical lesions in patients with corticobasal degeneration. Neurosci Lett 1999; 268: 5-8.
99. Saper CB, Wainer BH, German DC. Axonal and transneural transport in the transmission of neurological disease: Potential role in system degenerations including Alzheimer's disease. Neurosci 1987; 23: 389-398.
100. Matsumoto R, Nakamo I, Arai N, Oda M, Yagishita S, Hashyume Y. Loss of dentate nucleus neurons is associated with torpedo formation: A morphometric study in progressive supranuclear palsy and dentatonitropallidoluysian atrophy. Acta Neuropathol 1998; 95: 149-153.
101. Dickson DW, Feany MB, Yen SH, Mattiace LA, Davies P. Cytoskeletal pathology in non-Alzheimer degenerative dementia: New lesions in diffuse Lewy body disease, Pick's disease and corticobasal degeneration. J Neural Transm (Suppl) 1996; 47: 31-46.
102. Mori H, Oda M. Ballooned neurons in corticobasal degeneration and progressive supranuclear palsy. Neuropathology 1997; 17: 248-252.
103. Freiesleben W, Soylemezoglu F, Lowe J, Janzer RC, Kleihues P. Wernicke's encephalopathy with ballooned neurons in the mamillary bodies: An immunohistochemical study. Neuropath Appl Neurobiol 1997; 23: 36-42.
104. Ikemoto A, Hirano A, Matsumoto S, Akiguchi I, Kimura J. Synaptophysin expression in the anterior horn of Werdnig-Hoffman disease. J Neurol Sci 1996; 136: 94-100.
105. Kato S, Hirano A, Umahara T, Llena JF, Herz F, Ohama E. Ultrastructural and immunohistochernical studies on ballooned cortical neurons in Creutzfeldt-Jakob disease: Expression of alpha-B-crystallin, ubiquitin and stress response protein-27. Acta Neuropathol 1992; 84: 443-448.