Neuropathology of Parkinson's disease

Journal of Neuropathology and Experimental Neurology

Volumn 55, Issue 3, 1996, Pages 259-272

  Forno, Lysia S ^a  

^a VA PALO ALTO HEALTH CARE SYSTEM   (United States)

Author keywords

Basal ganglia; Cytoskeleton; Lewy bodies; Parkinsonism; Substantia nigra

Indexed keywords

LEVODOPA;

BRAIN SURGERY; CLINICAL FEATURE; ENVIRONMENTAL FACTOR; GENETIC SUSCEPTIBILITY; GLOBUS PALLIDUS; HUMAN; LEWY BODY; NERVE DEGENERATION; NIGRONEOSTRIATAL SYSTEM; NONHUMAN; PARKINSON DISEASE; PATHOGENESIS; PRIORITY JOURNAL; REVIEW; SUBSTANTIA NIGRA; TREATMENT PLANNING;

EID: 0029981526     PISSN: 00223069     EISSN: None     Source Type: Journal    
DOI: 10.1097/00005072-199603000-00001     Document Type: Review

References (101)

1. Parkinson J, An essay on the shaking palsy. London. 1817. Reproduced in: Critchley M, ed. James Parkinson. London: Macmillan, 1955
2. Charcot JM, Lectures on the diseases of the nervous system. Translated by Sigerson G. London: The New Sydenham Society, 1877
3. Stern G. James Parkinson 1755-1824. In: Stern G, ed. Parkinson's disease London: Chapman and Hall Medical, 1990:xiii-xxvii
4. Lewy FH. Paralysis agitans. I pathologische anatomie. In: Lewandowsky M, ed. Handbuch der Neurologie. Berlin: Springer, 1912: 920-33
5. Lewy FH. Die Lehre vom Tonus und der Bewegung. Berlin: Springer, 1923
6. Stern G. The effects of lesions in the substantia nigra Brain 1966;89:449-87
7. Lamy P. Paralysie agitante. In: Charcot JM, Brissaud E, Bouchard G, eds. Le traite de medecine. Paris: Masson, 1994:1270-76
8. Brissaud F. Clinique des maladies du systeme nerveux. Sur la nature et la pathogenie de la maladie de Parkinson. Journal de medicine et la chirurgie pratique 1895;65:641-63
9. Aita JF, Aita JA, O'Connell BL. Historical neurology. Maladie de Parkinson unilateral: Symptomatique d'une tumeur de pedoncule cerebral. Neurology 1987;37:1145-4-9
10. Vogt C, Vogt O. Zur lehre der erkrankungen des striaren systems. Journal fur Psychologie und Neurologie 1920;25(supp13):627-845
11. Tretiakoff C. Contribution a l'etude de l'anatomie pathologique du locus niger de Soemmering avec quelques deductions relatives a la pathogenie des troubles du tonus musculaires et de la maladie de Parkinson. Thesis. University of Paris, 1919
12. Foix C, Nicolesco J. Les noyaux gris centraux et la region mesencephale-sous-optique. Paris: Masson, 1925
13. Freeman W. The pathology of paralysis agitans. Ann Clin Med 1925;4:106-16
14. Hassler R. Zur Pathologie der Paralysis agitans und des postenzeplialitischen Parkinsonismus. Journal fur Psychologie und Neurologie 1938;48:387-486
15. Klaue R. Parkinsonische Krankheit (Paralysis agitans) und postencephalitischer Parkinsonismus. Versuch einer klinisch-anatomischen differentialdiagnose. Archiv fur Psychiatrie und Nervenkrankheiten 1940;111:251-321
16. Greenfield JG, Bosanquet FD. The brain-stem lesions in parkinsonism. J Neurol Neurosurg Psychiatry 1953;16:213-26
17. Mettler FA. Substantia nigra and parkinsonism. Arch Neurol 1964;10:529-42
18. Denny-Brown D. The basal ganglia and their relation to disorders of movement. Oxford: Oxford University Press, 1962
19. Ehringer H, Hornykiewicz O. Verteiling von Noradrenalin und Dopamine (3-Hydroxytyramin) in gehirn des menschen und ihr verhalten bei erkrankungen des extrapyramidales system. Klini sehe Wochenschrift 1960;38:1236-39
20. Anden NE, Carlsson A, Dahlstrom A, Fuxe K, Hillarp NA, Larsson K. Demonstration and mapping out of nigro-neostriatal dopamine neurons. Life Sci 1964;3:523-30
21. Carlsson A. Summation of the conference and conclusions. In: Barbeau A, McDowell F, eds. L-Dopa and parkinsonism. Philadelphia: F. A. Davis Company, 1970:413-17
22. Barbeau A. Parkinson's disease: Clinical features and etiopathology. In: Vinken PJ, Bruyn GW, Klawans HL. Handbook of clinical neurology. Extrapyramidal disorders. Amsterdam: Elsevier Science Publishers, 1986;5:87-152
23. Yahr MD, Parkinson's disease. The L-Dopa era. In: Narabayashi H, Nagatsu T, Yanigasawa N, Mizuno Y, eds. Parkinson's disease. From basic research to treatment. Adv Neurol 1993;60:11-17
24. Reyes P, Seestedt R, Golden G, Rice J, Arbizo V. Lewy bodies in olfactory bulbs in Alzheimer's disease and in Parkinson's disease. (Abstract) J Neuropathol Exp Neurol 1992;51:327
25. Jager, WA den Hartog, Bethlem J. The distribution of Lewy bodies in the central and autonomie nervous system in idiopathic paralysis agitans. J Neurol Ncurosurg Psychiatry 1960;23:283-90
26. Rajput AH, Rozdilsky B, Rajput A. Accuracy of clinical diagnosis in parkinsonism - A prospective study. Canad J Neurol Sci 1991;18:275-78
27. Hughes AJ, Daniel SE, Kilford L, Lecs AJ. Accuracy of the clinical diagnosis of idiopathic Parkinson's disease: A clinicopathological study of 100 cases J Neurol Neurosurg Psychiatry 1992;55:181-84
28. Zack MM, Langston JW. Is Parkinson's disease a single entity with a single cause? A cautionary note. In: Ellenberg JH, Koller WC, Langston JW, eds. Etiology of Parkinson's disease. New York: Marcel Dekker, 1995:55-63
29. Alvord EC, Forno LS, Kusske JA, Kauffman RJ, Rhodes JS, Goetowski CR. The pathology of parkinsonism: A comparison of degenerations in cerebral cortex and brainstem. Adv Neurol 1974;5: 175-93
30. Rajput AH, Uitti RJ, Sudhakar S, Rozdilsky B. Parkinsonism and neurofibrillary tangle pathology in pigmented nuclei. Ann Neurol 1989;25:602-6
31. Pollanen MS, Dickson DW, Bergeron C. Pathology and biology of the Lewy body. J Neuropathol Exp Neurol 1993;52:183-89
32. Forno LS. The Lewy body in Parkinson's disease. Adv Neurol 1986;45:35-43
33. Gibb WRG, Scott T, Lees AJ. Neuronal inclusions of Parkinson's disease. Movement Disorders 1991;6:2-11
34. Langston JW, Forno LS. The hypothalamus in Parkinson's disease. Ann Neurol 1978;3:129-33
35. Forno LS, Norville RL. The ultrastructure of Lewy bodies in the stellate ganglion. Acta Neuropathol 1976;34:183-97
36. Pollanen MS, Bergeron C, Weyer L. Detergent-insoluble cortical Lewy body fibrils share epitopes with neurofilament and tau. J Ncurochcm 1992;58:1953-56
37. Galloway PG, Grundke-Iqbal I, Iqbal K, Perry G. Lewy bodies contain epitopes both shared and distinct from Alzheimer's neurofibrillary tangles. J Neuropathol Exp Neurol 1988;47:654-63
38. Jellinger K. New developments in the pathology of Parkinson's disease. Adv Neurol 1990;53:1-16
39. Forrio LS. Pathological considerations in the etiology of Parkinson's disease. In: Ellenberg JH, Koller WH, Langston JW, eds. Etiology of Parkinson's disease. New York: Marcel Dekker, Inc., 1995:65-95
40. Hill WD, Lee VM-Y, Hurting HI, Murray JM, Trojanowski JQ. Epitopes located in spatially separate domains of each neurofilament subunit are present in Parkinson's disease Lewy bodies. J Comp Neurol 1991;309:150-60
41. Lennox J, Lowe J, Morrell K, Landon M, Mayer RJ. Anti-ubiquitin immunocytochemistry is more sensitive than conventional techniques in the detection of diffuse Lewy body disease. J Neurol Neurosurg Psychiatry 1989;52:67-71
42. Galloway PG, Bergeron C, Perry G. The presence of tau distinguishes Lewy bodies of diffuse Lewy body disease from those of idiopathic Parkinson's disease. Neurosci Lett 1989;100:6-10
43. Forno LS, DeLanney LE, Irwin I, Langston JW. Electron microscopy of Lewy bodies in the amygdala-parahippocampal region. Comparison with inclusion bodies in the MPTP-treated squirrel monkey. In: Battistin L, Scarlato G, Caraceni T, Ruggieri S, eds. Parkinson's disease. Philadelphia: Lippincott-Raven Publishers. Adv Neurol 1996;69:217-28
44. Lowe J, McDermott H, Landon M, Mayer RJ, Wilkinson KD. Ubiquitin carboxyl-terminal hydrolase (PGP 9.5) is selectively present in ubiquitinated inclusion bodies characteristic of human neurodegenerative diseases. J Pathol 1990;153-60
45. Iwatsubo T, Yamaguchi H, Fujimuro M, Yokosawa H, Ihara Y, Trojanowski Q, Lee VM-Y. Lewy body purification from diffuse Lewy body disease brains and identification of Lewy body-assòciated polyubiquitin chains. (Abstract) Movement Disorders 1995;10:688
46. Montine TJ, Farris DB, Graham DG. Covalent crosslinking of neurofilament protein by oxidized catechols as a potential mechanism of Lewy body formation. J Neuropathol Exp Neurol 1995;54:311-19
47. Bernheimer H, Birkmayer W, Hornykiewicz O, Jellinger K, Scitelberger F Brain dopamine and the syndromes of Parkinson and Huntington. J Neurol Sci 1973;20:415-55
48. Beheim-Schwarzbach D. Uber Zellleibveranderungen im Nucleus coeruleus bei Parkinsonsymptomen J Nerv Ment Dis 1952;116: 619-32
49. Lipkin LE. Cytoplasmic inclusions in ganglion cells associated with parkinsonian states. A neurocellular change studied in 53 cases and 206 controls. Amer J Pathol 1959;35:1117-33
50. Forno LS. Concentric hyalin intraneuronal inclusions of Lewy type in the brains of elderly persons (50 incidental cases): Relationship to Parkinsonism. J Amer Geriat Soc 1969;17:557-75
51. Ditter SM, Mirra SS. Neuropathological and clinical features of Parkinson's disease in Alzheimer's disease patients. Neurology 1987;37:754-60
52. Kosaka K, Yoshimura M, Ikeda K, Budka H. Diffuse type of Lewy body disease: Progressive dementia with abundant cortical Lewy bodies - A new disease? Clin Neuropathol 1984:185-92
53. Okazaki H, Lipkin LE, Aronson SM. Diffuse intracytoplasmic ganglionic inclusions (Lewy type) associated with progressive dementia and quadriparesis in flexion. J Neuropathol Exp Neurol 1961;20:237-44
54. Woodard JS. Concentric hyalin inclusion body formation in mental disease. Analysis of 27 cases. J Neuropathol Exp Neurol 1962;21:442-9
55. Bergeron C, Pollanen M. Lewy bodies in Alzheimer's disease - One or two diseases. Alzheimer Dis Assoc Disord 1989;3:197-204
56. Jellinger K. Morphology of Alzheimer's disease and related disorders. In: Maurer K, Riederer P, Beckmann H, eds. Alzheimer's disease Epidemiology, neuropathology, neurochemistry and clinics. Wien, New York: Springer-Verlag, 1990:61-77
57. Forno LS, Langston JW. Lewy bodies and aging: Relation to Alzheimer's and Parkinson's diseases. Neurodegeneration 1993;2:19-24
58. Hansen L, Salmon D, Galasko D, et al. The Lewy body variant of Alzheimer's disease: A clinical and pathologic study. Neurology 1990;40:1-8
59. Forno LS. Neuropathologic features of Parkinson's, Huntington's and Alzheimer's diseases. NYAS 1992;648:6-16
60. Spellman GG. Report of familial cases of parkinsonism. JAMA 1962;179:160-62
61. Muenter MD, Howard FM, Okazaki H, Forno LS, Kish SJ, Hornykiewicz O. A familial parkinson-dementia syndrome. (Abstract) Neurology 1986;36:115
62. Galloway PG, Perry G. Tropomyosin distinguishes Lewy bodies of Parkinson's disease from other neurofibrillary pathology. Brain Res 1991;541:347-49
63. Smith MA, Perry G. Is a Lewy body always a Lewy body? In: Korczyn AD, ed. Dementia in Parkinson's disease. Bologna, Italy Monduzzi Editore, 1995:187-93
64. Dickson DW, Ruan D, Crystal H, Mark MH, Davies P, Kress Y, Yen S-H. Hippocampal degeneration differentiates diffuse Lewy body disease (DLBD) from Alzheimer's disease: Light and electron microscopic immunocytochemistry of CA 2-3 neurites specific to DLBD. Neurology 1991;41:1402-9
65. Dickson DW, Schmidt ML, Lee VM-Y, Zhao M-L, Yen S-H, Trojanowski JQ. Immunoreactivity profile of hippocampal CA2/3 neurites in diffuse Lewy body disease. Acta Neuropathol (Berlin) 1994;86:269-76
66. Kim H, Gearing M, Mirra SS. Ubiquitin-positive CA2/3 neurites in hippocampus coexist with Lewy bodies. Neurology 1995;45: 1768-70
67. Beck BJ. Neuropsychiatrie manifestations of diffuse Lewy body disease. J Geriatr Psychiatry Neurol 1995;8:189-96
68. Gibb WRG, Lees AJ. The relevance of the Lewy body to the pathogenesis of idiopathic Parkinson's disease. J Neurol Neurosurg Psychiatry 1988;51:745-52
69. D'Amato CJ, Foster NL, Hicks SP, Sima AAF. Swollen cortical neurons and Lewy bodies accompanying progressive supranuclear palsy and Creutzfeldt-Jakob's disease. (Abstract) J Neuropathol Exp Neurol 1992;51:324
70. Gearing M, Olson DA, Watts RL, Mirra SS. Progressive supranuclear palsy. Neuropathologic and clinical heterogeneity. Neurology 1994;44:1015-24
71. Hirano A, Kurland LT, Sayre GP. Familial amyotrophic lateral sclerosis. A subgroup characterized by posterior and spinocerebellar tract involvement and hyaline inclusions in the anterior horn cells. Arch Neurol 1967;16:232-43
72. Takahashi K, Nakamura HD, Okada E. Hereditary amyotrophic lateral sclerosis. Histochemical and electron microscopic study of hyaline inclusions in motor neurons. Arch Neurol 1972;27: 292-99
73. Oda M, Akagawa N, Tabuchi Y, Tanabe H. A sporadic juvenile case of the amyotrophic lateral sclerosis with neuronal intracytoplasmic inclusions. Acta Neuropathol (Berlin) 1978:211-16
74. Maruyama S, Ookawa Y, Mori H, Nakano I, Ihara Y, Kuzuhara S, Tomonaga M. Immunocytochemical and ultrastructural study of Lewy body-like hyaline inclusions in familial amyotrophic lateral sclerosis. Acta Neuropathol (Berlin) 1989;78:143-52
75. Sasaki S, Maruyama S. Immunocytochemical and ultrastructural studies of hyaline inclusions in sporadic motor neuron disease. Acta Neuropathol 1991;82:295-301
76. Tranchant C, Dugay M-H, Mohr M, Wasser P, Warter J-M. Familial motor neuron disease with Lewy body-like inclusions in the substantia nigra, the subthalamic nucleus, and the globus pallidus. J Neurol Sci 1992:18-23
77. Lowe J. New pathological findings in amyotrophic lateral sclerosis. J Neurol Sci 1994;124(Suppl):38-51
78. Shibata N, Hirano A, Kobayashi M, et al. Cu/Zn superoxide dismutase-like immunoreactivity in Lewy body-like inclusions of sporadic amyotrophic lateral sclerosis. Neurosci Lett 1994;179: 149-52
79. Nishiyama N, Murayama S, Shimizu J, Ohya Y, Kwak S, Asayama K, Kanazawa I. Cu/Zn dismutase-like immunoreactivity is present in Lewy bodies from Parkinson's disease: A light and electron microscopic immunocytochemical study. Acta Neuropathol 1995;89:471-74
80. Ohama E, Ikuta F. Parkinson's disease; Distribution of Lewy bodies and monoamine neuron system. Acta Neuropathol (Berlin) 1976:311-19
81. Agid Y, Ruberg M, Javoy-Agid F, et al. Are dopaminergic neurons selectively vulnerable to Parkinson's disease? In: Narabayashi H, Nagatsu T, Yanigasawa N, Mizuno Y, eds. Parkinson's disease. From basic research to treatment. New York: Raven Press, Adv Neurol 1993;60:148-64
82. Gelman BB. Iron in CNS disease. J Neuropathol Exp Neurol 1995;54:477-86
83. Jellinger KA, Lienzl E, Rumpelmaier G, et al. Iron and ferritin in substantia nigra in Parkinson's disease. In: Narabayashi H, Nagatsu T, Yanigasawa N, Mizuno Y, eds. Parkinson's disease. From basic research to treatment. New York: Raven Press, Adv Neurol 1993;60:267-72
84. Good PF, Olanow CW, Perl DP. Neuromelanin-containing neurons of the substantia nigra accumulate iron and aluminum in Parkinson's disease: A LAMMA study. Brain Res 1992;593:343-46
85. Mizuno Y, Ikebe S-I, Hattori N, Kondo T, Tanaka M, Ozawa T. Mitochondrial energy crisis in Parkinson's disease. In: Narabayashi H, Nagatsu T, Yanigasawa N, Mizuno Y, eds. Parkinson's disease. From basic research to treatment. New York: Raven Press, Adv Neurol 1993;60:282-87
86. Schapira AHV. Mitochondria complex I deficiency in Parkinson's disease. In: Narabayashi H, Nagatsu T, Yanigasawa N, Mizuno Y, eds. Parkinson's disease. From basic research to treatment. New York. Raven Press, Adv Neurol 1993;60:288-91
87. Tompkins MM, Hill WD. Apoptotic-like changes in human substantia nigra. (Abstract) Soc Neurosci 1995;21:1273
88. Anglade P, Vyas S, Javoi-Agid F, et al. Apoptotic degeneration of nigral dopaminergic neurons in Parkinson's disease. (Abstract) Soc Neurosci 1995;21:1250
89. Mann DMA, Yates PO. Possible role of neuromelanin in the pathogenesis of Parkinson's disease. Mech Ageing Dev 1983;21: 193-203
90. Hirsch E, Graybiel AM, Agid YA. Mclanized dopaminergic neurons are differentially susceptible to degeneration in Parkinson's disease. Nature 1988;334:345-48
91. Fearnley JM, Lees AJ. Aging and Parkinson's disease: Substantia nigra regional selectivity. Brain 1991;114:2283-2301
92. TINS. Special issue: Basal ganglia research, 1990;13(7):241-308
93. Shepherd GM. Neurobiology. New York, Oxford: Oxford University Press, 1994
94. Parent A, Hazrati L-N. Functional anatomy of the basal ganglia. I. The cortico-basal ganglia-thalamo-cortical loop. Brain Res Rev 1995;20:91-127
95. Parent A, Hazrati L-N. Functional anatomy of the basal ganglia. II. The place of subthalamic nucleus and external pallidum in basal ganglia circuitry. Brain Res Rev 1995:128-54
96. Wichmann T, Vitek JL, DeLong M. Parkinson's disease and the basal ganglia: Lessons from the laboratory and from neurosurgery. The Neuroscientist 1955;1:236-44
97. Langston JW. MPTP as it relates to the etiology of Parkinson's disease. In: Ellenberg JH, Koller WH, Langston JW, eds. Etiology of Parkinson's disease. New York: Marcel Dekker, Inc., 1995:367-99
98. Forno LS, DeLanney LE, Irwin I, Langston JW. Similarities and differences between MPTP-induced parkinsonism and Parkinson's disease. Neuropathologic considerations. In: Narabayashi H, Nagatsu T, Yanigasawa N, Mizuno Y, eds. Parkinson's disease. From basic research to treatment. New York: Raven Press, Adv Neurol 1993;60:600-608
99. Davies RW, Sutcliffe RG, Shiels P, Alonso MD, Clarke DJ, Gilmore D, Payne AP. Characterization of a mouse mutant with similarities to Parkinson's disease. Soc Neurosci Abstracts 1995;21: 1244
100. Duvoisin RC, Johnson WG. Hereditary Lewy-body parkinsonism and evidence for a genetic etiology of Parkinson's disease. Brain Pathology 1992;2:309-20
101. Duvoisin RC, Golbe LI. Kindreds of dominantly inherited Parkinson's disease: Keys to the riddle. Ann Neurol 1995;38:355-56